Single Cell Profiling of Circulating Tumor Cells: Transcriptional Heterogeneity and Diversity from Breast Cancer Cell Lines

To improve cancer therapy, it is critical to target metastasizing cells. Circulating tumor cells (CTCs) are rare cells found in the blood of patients with solid tumors and may play a key role in cancer dissemination. Uncovering CTC phenotypes offers a potential avenue to inform treatment. However, C...

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Vydáno v:	PloS one Ročník 7; číslo 5; s. e33788
Hlavní autoři:	Powell, Ashley A., Talasaz, AmirAli H., Zhang, Haiyu, Coram, Marc A., Reddy, Anupama, Deng, Glenn, Telli, Melinda L., Advani, Ranjana H., Carlson, Robert W., Mollick, Joseph A., Sheth, Shruti, Kurian, Allison W., Ford, James M., Stockdale, Frank E., Quake, Stephen R., Pease, R. Fabian, Mindrinos, Michael N., Bhanot, Gyan, Dairkee, Shanaz H., Davis, Ronald W., Jeffrey, Stefanie S.
Médium:	Journal Article
Jazyk:	angličtina
Vydáno:	United States Public Library of Science 07.05.2012 Public Library of Science (PLoS)
Témata:	Analysis Antigens Biochemistry Bioengineering Biology Biopsy Biotechnology Blood Blood circulation Breast cancer Breast Neoplasms - blood Breast Neoplasms - genetics Breast Neoplasms - metabolism Cancer Cancer metastasis Cancer treatment Cell Line, Tumor Contamination CXCR4 protein Drug discovery Electrical engineering Engineering Epidermal growth factor Feasibility studies Female Gene expression Gene Expression Profiling Gene Expression Regulation, Neoplastic Genes Genetic aspects Genomes Health aspects Heterogeneity Humans Kinases Leukocytes Lymphoma - blood Medical research Medicine Mesenchyme Metastases Metastasis Microarray Analysis - methods Microfluidic Analytical Techniques Microfluidics Molecular biology Motility Neoplasm Metastasis Neoplastic Cells, Circulating - metabolism Pancreatic cancer Patients Prostate Rodents S100A4 protein Single-Cell Analysis - instrumentation Single-Cell Analysis - methods Solid tumors Stem cells Subgroups Surgery Therapy Transcription Transcription (Genetics) Transforming growth factors Tumor cell lines Tumor cells Tumors Palo Alto California California United States > US New Brunswick New Jersey
ISSN:	1932-6203, 1932-6203
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Abstract	To improve cancer therapy, it is critical to target metastasizing cells. Circulating tumor cells (CTCs) are rare cells found in the blood of patients with solid tumors and may play a key role in cancer dissemination. Uncovering CTC phenotypes offers a potential avenue to inform treatment. However, CTC transcriptional profiling is limited by leukocyte contamination; an approach to surmount this problem is single cell analysis. Here we demonstrate feasibility of performing high dimensional single CTC profiling, providing early insight into CTC heterogeneity and allowing comparisons to breast cancer cell lines widely used for drug discovery. We purified CTCs using the MagSweeper, an immunomagnetic enrichment device that isolates live tumor cells from unfractionated blood. CTCs that met stringent criteria for further analysis were obtained from 70% (14/20) of primary and 70% (21/30) of metastatic breast cancer patients; none were captured from patients with non-epithelial cancer (n = 20) or healthy subjects (n = 25). Microfluidic-based single cell transcriptional profiling of 87 cancer-associated and reference genes showed heterogeneity among individual CTCs, separating them into two major subgroups, based on 31 highly expressed genes. In contrast, single cells from seven breast cancer cell lines were tightly clustered together by sample ID and ER status. CTC profiles were distinct from those of cancer cell lines, questioning the suitability of such lines for drug discovery efforts for late stage cancer therapy. For the first time, we directly measured high dimensional gene expression in individual CTCs without the common practice of pooling such cells. Elevated transcript levels of genes associated with metastasis NPTN, S100A4, S100A9, and with epithelial mesenchymal transition: VIM, TGFß1, ZEB2, FOXC1, CXCR4, were striking compared to cell lines. Our findings demonstrate that profiling CTCs on a cell-by-cell basis is possible and may facilitate the application of 'liquid biopsies' to better model drug discovery.
AbstractList	Background To improve cancer therapy, it is critical to target metastasizing cells. Circulating tumor cells (CTCs) are rare cells found in the blood of patients with solid tumors and may play a key role in cancer dissemination. Uncovering CTC phenotypes offers a potential avenue to inform treatment. However, CTC transcriptional profiling is limited by leukocyte contamination; an approach to surmount this problem is single cell analysis. Here we demonstrate feasibility of performing high dimensional single CTC profiling, providing early insight into CTC heterogeneity and allowing comparisons to breast cancer cell lines widely used for drug discovery. Methodology/Principal Findings We purified CTCs using the MagSweeper, an immunomagnetic enrichment device that isolates live tumor cells from unfractionated blood. CTCs that met stringent criteria for further analysis were obtained from 70% (14/20) of primary and 70% (21/30) of metastatic breast cancer patients; none were captured from patients with non-epithelial cancer (n = 20) or healthy subjects (n = 25). Microfluidic-based single cell transcriptional profiling of 87 cancer-associated and reference genes showed heterogeneity among individual CTCs, separating them into two major subgroups, based on 31 highly expressed genes. In contrast, single cells from seven breast cancer cell lines were tightly clustered together by sample ID and ER status. CTC profiles were distinct from those of cancer cell lines, questioning the suitability of such lines for drug discovery efforts for late stage cancer therapy. Conclusions/Significance For the first time, we directly measured high dimensional gene expression in individual CTCs without the common practice of pooling such cells. Elevated transcript levels of genes associated with metastasis NPTN, S100A4, S100A9, and with epithelial mesenchymal transition: VIM, TGFß1, ZEB2, FOXC1, CXCR4, were striking compared to cell lines. Our findings demonstrate that profiling CTCs on a cell-by-cell basis is possible and may facilitate the application of ‘liquid biopsies’ to better model drug discovery. To improve cancer therapy, it is critical to target metastasizing cells. Circulating tumor cells (CTCs) are rare cells found in the blood of patients with solid tumors and may play a key role in cancer dissemination. Uncovering CTC phenotypes offers a potential avenue to inform treatment. However, CTC transcriptional profiling is limited by leukocyte contamination; an approach to surmount this problem is single cell analysis. Here we demonstrate feasibility of performing high dimensional single CTC profiling, providing early insight into CTC heterogeneity and allowing comparisons to breast cancer cell lines widely used for drug discovery. We purified CTCs using the MagSweeper, an immunomagnetic enrichment device that isolates live tumor cells from unfractionated blood. CTCs that met stringent criteria for further analysis were obtained from 70% (14/20) of primary and 70% (21/30) of metastatic breast cancer patients; none were captured from patients with non-epithelial cancer (n = 20) or healthy subjects (n = 25). Microfluidic-based single cell transcriptional profiling of 87 cancer-associated and reference genes showed heterogeneity among individual CTCs, separating them into two major subgroups, based on 31 highly expressed genes. In contrast, single cells from seven breast cancer cell lines were tightly clustered together by sample ID and ER status. CTC profiles were distinct from those of cancer cell lines, questioning the suitability of such lines for drug discovery efforts for late stage cancer therapy. For the first time, we directly measured high dimensional gene expression in individual CTCs without the common practice of pooling such cells. Elevated transcript levels of genes associated with metastasis NPTN, S100A4, S100A9, and with epithelial mesenchymal transition: VIM, TGFß1, ZEB2, FOXC1, CXCR4, were striking compared to cell lines. Our findings demonstrate that profiling CTCs on a cell-by-cell basis is possible and may facilitate the application of 'liquid biopsies' to better model drug discovery. Background To improve cancer therapy, it is critical to target metastasizing cells. Circulating tumor cells (CTCs) are rare cells found in the blood of patients with solid tumors and may play a key role in cancer dissemination. Uncovering CTC phenotypes offers a potential avenue to inform treatment. However, CTC transcriptional profiling is limited by leukocyte contamination; an approach to surmount this problem is single cell analysis. Here we demonstrate feasibility of performing high dimensional single CTC profiling, providing early insight into CTC heterogeneity and allowing comparisons to breast cancer cell lines widely used for drug discovery. Methodology/Principal Findings We purified CTCs using the MagSweeper, an immunomagnetic enrichment device that isolates live tumor cells from unfractionated blood. CTCs that met stringent criteria for further analysis were obtained from 70% (14/20) of primary and 70% (21/30) of metastatic breast cancer patients; none were captured from patients with non-epithelial cancer (n = 20) or healthy subjects (n = 25). Microfluidic-based single cell transcriptional profiling of 87 cancer-associated and reference genes showed heterogeneity among individual CTCs, separating them into two major subgroups, based on 31 highly expressed genes. In contrast, single cells from seven breast cancer cell lines were tightly clustered together by sample ID and ER status. CTC profiles were distinct from those of cancer cell lines, questioning the suitability of such lines for drug discovery efforts for late stage cancer therapy. Conclusions/Significance For the first time, we directly measured high dimensional gene expression in individual CTCs without the common practice of pooling such cells. Elevated transcript levels of genes associated with metastasis NPTN, S100A4, S100A9, and with epithelial mesenchymal transition: VIM, TGFß1, ZEB2, FOXC1, CXCR4, were striking compared to cell lines. Our findings demonstrate that profiling CTCs on a cell-by-cell basis is possible and may facilitate the application of 'liquid biopsies' to better model drug discovery. To improve cancer therapy, it is critical to target metastasizing cells. Circulating tumor cells (CTCs) are rare cells found in the blood of patients with solid tumors and may play a key role in cancer dissemination. Uncovering CTC phenotypes offers a potential avenue to inform treatment. However, CTC transcriptional profiling is limited by leukocyte contamination; an approach to surmount this problem is single cell analysis. Here we demonstrate feasibility of performing high dimensional single CTC profiling, providing early insight into CTC heterogeneity and allowing comparisons to breast cancer cell lines widely used for drug discovery.BACKGROUNDTo improve cancer therapy, it is critical to target metastasizing cells. Circulating tumor cells (CTCs) are rare cells found in the blood of patients with solid tumors and may play a key role in cancer dissemination. Uncovering CTC phenotypes offers a potential avenue to inform treatment. However, CTC transcriptional profiling is limited by leukocyte contamination; an approach to surmount this problem is single cell analysis. Here we demonstrate feasibility of performing high dimensional single CTC profiling, providing early insight into CTC heterogeneity and allowing comparisons to breast cancer cell lines widely used for drug discovery.We purified CTCs using the MagSweeper, an immunomagnetic enrichment device that isolates live tumor cells from unfractionated blood. CTCs that met stringent criteria for further analysis were obtained from 70% (14/20) of primary and 70% (21/30) of metastatic breast cancer patients; none were captured from patients with non-epithelial cancer (n = 20) or healthy subjects (n = 25). Microfluidic-based single cell transcriptional profiling of 87 cancer-associated and reference genes showed heterogeneity among individual CTCs, separating them into two major subgroups, based on 31 highly expressed genes. In contrast, single cells from seven breast cancer cell lines were tightly clustered together by sample ID and ER status. CTC profiles were distinct from those of cancer cell lines, questioning the suitability of such lines for drug discovery efforts for late stage cancer therapy.METHODOLOGY/PRINCIPAL FINDINGSWe purified CTCs using the MagSweeper, an immunomagnetic enrichment device that isolates live tumor cells from unfractionated blood. CTCs that met stringent criteria for further analysis were obtained from 70% (14/20) of primary and 70% (21/30) of metastatic breast cancer patients; none were captured from patients with non-epithelial cancer (n = 20) or healthy subjects (n = 25). Microfluidic-based single cell transcriptional profiling of 87 cancer-associated and reference genes showed heterogeneity among individual CTCs, separating them into two major subgroups, based on 31 highly expressed genes. In contrast, single cells from seven breast cancer cell lines were tightly clustered together by sample ID and ER status. CTC profiles were distinct from those of cancer cell lines, questioning the suitability of such lines for drug discovery efforts for late stage cancer therapy.For the first time, we directly measured high dimensional gene expression in individual CTCs without the common practice of pooling such cells. Elevated transcript levels of genes associated with metastasis NPTN, S100A4, S100A9, and with epithelial mesenchymal transition: VIM, TGFß1, ZEB2, FOXC1, CXCR4, were striking compared to cell lines. Our findings demonstrate that profiling CTCs on a cell-by-cell basis is possible and may facilitate the application of 'liquid biopsies' to better model drug discovery.CONCLUSIONS/SIGNIFICANCEFor the first time, we directly measured high dimensional gene expression in individual CTCs without the common practice of pooling such cells. Elevated transcript levels of genes associated with metastasis NPTN, S100A4, S100A9, and with epithelial mesenchymal transition: VIM, TGFß1, ZEB2, FOXC1, CXCR4, were striking compared to cell lines. Our findings demonstrate that profiling CTCs on a cell-by-cell basis is possible and may facilitate the application of 'liquid biopsies' to better model drug discovery. To improve cancer therapy, it is critical to target metastasizing cells. Circulating tumor cells (CTCs) are rare cells found in the blood of patients with solid tumors and may play a key role in cancer dissemination. Uncovering CTC phenotypes offers a potential avenue to inform treatment. However, CTC transcriptional profiling is limited by leukocyte contamination; an approach to surmount this problem is single cell analysis. Here we demonstrate feasibility of performing high dimensional single CTC profiling, providing early insight into CTC heterogeneity and allowing comparisons to breast cancer cell lines widely used for drug discovery. We purified CTCs using the MagSweeper, an immunomagnetic enrichment device that isolates live tumor cells from unfractionated blood. CTCs that met stringent criteria for further analysis were obtained from 70% (14/20) of primary and 70% (21/30) of metastatic breast cancer patients; none were captured from patients with non-epithelial cancer (n = 20) or healthy subjects (n = 25). Microfluidic-based single cell transcriptional profiling of 87 cancer-associated and reference genes showed heterogeneity among individual CTCs, separating them into two major subgroups, based on 31 highly expressed genes. In contrast, single cells from seven breast cancer cell lines were tightly clustered together by sample ID and ER status. CTC profiles were distinct from those of cancer cell lines, questioning the suitability of such lines for drug discovery efforts for late stage cancer therapy. For the first time, we directly measured high dimensional gene expression in individual CTCs without the common practice of pooling such cells. Elevated transcript levels of genes associated with metastasis NPTN, S100A4, S100A9, and with epithelial mesenchymal transition: VIM, TGFß1, ZEB2, FOXC1, CXCR4, were striking compared to cell lines. Our findings demonstrate that profiling CTCs on a cell-by-cell basis is possible and may facilitate the application of 'liquid biopsies' to better model drug discovery.
Audience	Academic
Author	Advani, Ranjana H. Talasaz, AmirAli H. Coram, Marc A. Sheth, Shruti Ford, James M. Powell, Ashley A. Kurian, Allison W. Stockdale, Frank E. Bhanot, Gyan Zhang, Haiyu Quake, Stephen R. Deng, Glenn Mindrinos, Michael N. Telli, Melinda L. Mollick, Joseph A. Reddy, Anupama Dairkee, Shanaz H. Carlson, Robert W. Pease, R. Fabian Davis, Ronald W. Jeffrey, Stefanie S.
AuthorAffiliation	9 Simons Center for Systems Biology, Institute for Advanced Study, Princeton, New Jersey, United States of America 1 Department of Surgery, Stanford University School of Medicine, Stanford, California, United States of America 4 Department of Health Research and Policy (Biostatistics), Stanford University School of Medicine, Stanford, California, United States of America 6 Department of Medicine, Stanford University School of Medicine, Stanford, California, United States of America 10 California Pacific Medical Center Research Institute, San Francisco, California, United States of America 2 Stanford Genome Technology Center, Stanford University, Palo Alto, California, United States of America 3 Department of Electrical Engineering, Stanford University, Stanford, California, United States of America 7 Howard Hughes Medical Institute, Department of Bioengineering, Stanford University, Stanford, California, United States of America 8 Cancer Institute of New Jersey, New Brunswick, New Jersey, Unit
AuthorAffiliation_xml	– name: 2 Stanford Genome Technology Center, Stanford University, Palo Alto, California, United States of America – name: 5 BioMaPS Institute for Quantitative Biology, Department of Physics, Department of Molecular Biology and Biochemistry, Rutgers University, Piscataway, New Jersey, United States of America – name: 6 Department of Medicine, Stanford University School of Medicine, Stanford, California, United States of America – name: 8 Cancer Institute of New Jersey, New Brunswick, New Jersey, United States of America – name: 1 Department of Surgery, Stanford University School of Medicine, Stanford, California, United States of America – name: University of California, Merced, United States of America – name: 10 California Pacific Medical Center Research Institute, San Francisco, California, United States of America – name: 9 Simons Center for Systems Biology, Institute for Advanced Study, Princeton, New Jersey, United States of America – name: 3 Department of Electrical Engineering, Stanford University, Stanford, California, United States of America – name: 4 Department of Health Research and Policy (Biostatistics), Stanford University School of Medicine, Stanford, California, United States of America – name: 7 Howard Hughes Medical Institute, Department of Bioengineering, Stanford University, Stanford, California, United States of America
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BackLink	https://www.ncbi.nlm.nih.gov/pubmed/22586443$$D View this record in MEDLINE/PubMed
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Conceived and designed the experiments: SSJ AAP AHT HZ SHD MNM SRQ RFP RWD. Performed the experiments: AAP HZ GD. Analyzed the data: MAC AR GB HZ SSJ SHD. Contributed reagents/materials/analysis tools: MLT RHA RWC JAM SS AWK JMF FES SRQ. Wrote the paper: SSJ SHD AAP AHT MNM HZ. Invented the MagSweeper: AHT AAP MNM RFP RWD SSJ. Optimized MagSweeper configuration and performance: AAP AHT. Current address: Department of Obstetrics and Gynecology, Stanford University School of Medicine, Stanford, California, United States of America Current address: Novartis Institutes for Biomedical Research, Cambridge, Massachusetts, United States of America Current address: Cancer Research Institute, College of Medicine, Xiangfan University, Xiangyang, Hubei, China Current address: Department of Diagnostic Research, Illumina, Inc., Hayward, California, United States of America
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Snippet	To improve cancer therapy, it is critical to target metastasizing cells. Circulating tumor cells (CTCs) are rare cells found in the blood of patients with... Background To improve cancer therapy, it is critical to target metastasizing cells. Circulating tumor cells (CTCs) are rare cells found in the blood of... Background To improve cancer therapy, it is critical to target metastasizing cells. Circulating tumor cells (CTCs) are rare cells found in the blood of...
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StartPage	e33788
SubjectTerms	Analysis Antigens Biochemistry Bioengineering Biology Biopsy Biotechnology Blood Blood circulation Breast cancer Breast Neoplasms - blood Breast Neoplasms - genetics Breast Neoplasms - metabolism Cancer Cancer metastasis Cancer treatment Cell Line, Tumor Contamination CXCR4 protein Drug discovery Electrical engineering Engineering Epidermal growth factor Feasibility studies Female Gene expression Gene Expression Profiling Gene Expression Regulation, Neoplastic Genes Genetic aspects Genomes Health aspects Heterogeneity Humans Kinases Leukocytes Lymphoma - blood Medical research Medicine Mesenchyme Metastases Metastasis Microarray Analysis - methods Microfluidic Analytical Techniques Microfluidics Molecular biology Motility Neoplasm Metastasis Neoplastic Cells, Circulating - metabolism Pancreatic cancer Patients Prostate Rodents S100A4 protein Single-Cell Analysis - instrumentation Single-Cell Analysis - methods Solid tumors Stem cells Subgroups Surgery Therapy Transcription Transcription (Genetics) Transforming growth factors Tumor cell lines Tumor cells Tumors
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Title	Single Cell Profiling of Circulating Tumor Cells: Transcriptional Heterogeneity and Diversity from Breast Cancer Cell Lines
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Volume	7
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