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 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.
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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2012 Powell et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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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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