Single Cell Profiling of Circulating Tumor Cells: Transcriptional Heterogeneity and Diversity from Breast Cancer Cell Lines
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{"title"=>"Single cell profiling of Circulating tumor cells: Transcriptional heterogeneity and diversity from breast cancer cell lines", "type"=>"journal", "authors"=>[{"first_name"=>"Ashley A.", "last_name"=>"Powell", "scopus_author_id"=>"7202501725"}, {"first_name"=>"Amir Ali H.", "last_name"=>"Talasaz", "scopus_author_id"=>"16176403700"}, {"first_name"=>"Haiyu", "last_name"=>"Zhang", "scopus_author_id"=>"8859827000"}, {"first_name"=>"Marc A.", "last_name"=>"Coram", "scopus_author_id"=>"14065755100"}, {"first_name"=>"Anupama", "last_name"=>"Reddy", "scopus_author_id"=>"24559491100"}, {"first_name"=>"Glenn", "last_name"=>"Deng", "scopus_author_id"=>"7101932147"}, {"first_name"=>"Melinda L.", "last_name"=>"Telli", "scopus_author_id"=>"16064818700"}, {"first_name"=>"Ranjana H.", "last_name"=>"Advani", "scopus_author_id"=>"7003342788"}, {"first_name"=>"Robert W.", "last_name"=>"Carlson", "scopus_author_id"=>"35274579200"}, {"first_name"=>"Joseph A.", "last_name"=>"Mollick", "scopus_author_id"=>"6603027680"}, {"first_name"=>"Shruti", "last_name"=>"Sheth", "scopus_author_id"=>"55209076200"}, {"first_name"=>"Allison W.", "last_name"=>"Kurian", "scopus_author_id"=>"56730290700"}, {"first_name"=>"James M.", "last_name"=>"Ford", "scopus_author_id"=>"7402915714"}, {"first_name"=>"Frank E.", "last_name"=>"Stockdale", "scopus_author_id"=>"7005205252"}, {"first_name"=>"Stephen R.", "last_name"=>"Quake", "scopus_author_id"=>"7004146463"}, {"first_name"=>"R. Fabian", "last_name"=>"Pease", "scopus_author_id"=>"57197500248"}, {"first_name"=>"Michael N.", "last_name"=>"Mindrinos", "scopus_author_id"=>"6603048545"}, {"first_name"=>"Gyan", "last_name"=>"Bhanot", "scopus_author_id"=>"7004654825"}, {"first_name"=>"Shanaz H.", "last_name"=>"Dairkee", "scopus_author_id"=>"57189963791"}, {"first_name"=>"Ronald W.", "last_name"=>"Davis", "scopus_author_id"=>"36012646500"}, {"first_name"=>"Stefanie S.", "last_name"=>"Jeffrey", "scopus_author_id"=>"23569502400"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-84860601923", "sgr"=>"84860601923", "pui"=>"364751107", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pmid"=>"22586443", "doi"=>"10.1371/journal.pone.0033788"}, "id"=>"01957967-3870-38ee-94a9-810f5f58a382", "abstract"=>"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.", "link"=>"http://www.mendeley.com/research/single-cell-profiling-circulating-tumor-cells-transcriptional-heterogeneity-diversity-breast-cancer-1", "reader_count"=>424, "reader_count_by_academic_status"=>{"Unspecified"=>8, "Professor > Associate Professor"=>25, "Librarian"=>1, "Researcher"=>109, "Student > Doctoral Student"=>21, "Student > Ph. D. Student"=>126, "Student > Postgraduate"=>14, "Student > Master"=>40, "Other"=>19, "Student > Bachelor"=>33, "Lecturer"=>11, "Lecturer > Senior Lecturer"=>6, "Professor"=>11}, "reader_count_by_user_role"=>{"Unspecified"=>8, "Professor > Associate Professor"=>25, "Librarian"=>1, "Researcher"=>109, "Student > Doctoral Student"=>21, "Student > Ph. D. Student"=>126, "Student > Postgraduate"=>14, "Student > Master"=>40, "Other"=>19, "Student > Bachelor"=>33, "Lecturer"=>11, "Lecturer > Senior Lecturer"=>6, "Professor"=>11}, "reader_count_by_subject_area"=>{"Unspecified"=>15, "Agricultural and Biological Sciences"=>178, "Veterinary Science and Veterinary Medicine"=>1, "Chemical Engineering"=>3, "Chemistry"=>26, "Computer Science"=>8, "Engineering"=>53, "Biochemistry, Genetics and Molecular Biology"=>54, "Nursing and Health Professions"=>1, "Materials Science"=>1, "Mathematics"=>5, "Medicine and Dentistry"=>63, "Pharmacology, Toxicology and Pharmaceutical Science"=>2, "Physics and Astronomy"=>8, "Psychology"=>1, "Social Sciences"=>2, "Immunology and Microbiology"=>3}, "reader_count_by_subdiscipline"=>{"Materials Science"=>{"Materials Science"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>63}, "Social Sciences"=>{"Social Sciences"=>2}, "Physics and Astronomy"=>{"Physics and Astronomy"=>8}, "Psychology"=>{"Psychology"=>1}, "Mathematics"=>{"Mathematics"=>5}, "Unspecified"=>{"Unspecified"=>15}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>2}, "Chemical Engineering"=>{"Chemical Engineering"=>3}, "Engineering"=>{"Engineering"=>53}, "Chemistry"=>{"Chemistry"=>26}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>3}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>178}, "Computer Science"=>{"Computer Science"=>8}, "Nursing and Health Professions"=>{"Nursing and Health Professions"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>54}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"United States"=>13, "Japan"=>2, "United Kingdom"=>5, "Switzerland"=>2, "Portugal"=>1, "Spain"=>3, "Saudi Arabia"=>1, "Austria"=>1, "Netherlands"=>1, "Sweden"=>1, "South Korea"=>1, "Belgium"=>1, "Iran"=>1, "China"=>1, "Italy"=>1, "South Africa"=>2, "Mexico"=>1, "Israel"=>1, "France"=>2, "Nigeria"=>1, "Germany"=>2}, "group_count"=>25}

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  • {"files"=>["https://ndownloader.figshare.com/files/332037", "https://ndownloader.figshare.com/files/332087", "https://ndownloader.figshare.com/files/332159", "https://ndownloader.figshare.com/files/332205", "https://ndownloader.figshare.com/files/332245"], "description"=>"<div><h3>Background</h3><p>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.</p> <h3>Methodology/Principal Findings</h3><p>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.</p> <h3>Conclusions/Significance</h3><p>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 <em>NPTN, S100A4</em>, <em>S100A9</em>, and with epithelial mesenchymal transition: <em>VIM, TGFß1, ZEB2, FOXC1</em>, <em>CXCR4,</em> 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.</p> </div>", "links"=>[], "tags"=>["profiling", "circulating", "transcriptional", "heterogeneity", "cancer", "lines"], "article_id"=>125549, "categories"=>["Biological Sciences", "Biotechnology", "Cancer", "Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Ashley A. Powell", "AmirAli H. Talasaz", "Haiyu Zhang", "Marc A. Coram", "Anupama Reddy", "Glenn Deng", "Melinda L. Telli", "Ranjana H. Advani", "Robert W. Carlson", "Joseph A. Mollick", "Shruti Sheth", "Allison W. Kurian", "James M. Ford", "Frank E. Stockdale", "Stephen R. Quake", "R. Fabian Pease", "Michael N. Mindrinos", "Gyan Bhanot", "Shanaz H. Dairkee", "Ronald W. Davis", "Stefanie S. Jeffrey"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0033788.s001", "https://dx.doi.org/10.1371/journal.pone.0033788.s002", "https://dx.doi.org/10.1371/journal.pone.0033788.s003", "https://dx.doi.org/10.1371/journal.pone.0033788.s004", "https://dx.doi.org/10.1371/journal.pone.0033788.s005"], "stats"=>{"downloads"=>4, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Single_Cell_Profiling_of_Circulating_Tumor_Cells_Transcriptional_Heterogeneity_and_Diversity_from_Breast_Cancer_Cell_Lines/125549", "title"=>"Single Cell Profiling of Circulating Tumor Cells: Transcriptional Heterogeneity and Diversity from Breast Cancer Cell Lines", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-05-07 01:32:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/641641"], "description"=>"<p>A. Heatmap of single cell gene expression of 87 genes within seven individual cells isolated from three primary tumor-derived (pink: CCdl054, orange: CCdl672, gold: CCdl675), and four metastatic effusion-derived (red: MDA-231 plum: SKBR3, dark green: MCF7, and bright green: T47D) breast cancer cell lines. Yellow indicates high gene expression; gray is median expression; blue indicates low expression; and black represents undetectable expression. All cells showed expected expression patterns. The breast cancer cell lines used represent a spectrum of cell differentiation, e.g., from less differentiated and more mesenchymal/stem cell-like ER-negative (basal-like) cells (MDA-231 and SKBR3) to more differentiated ER-positive (luminal-like) cells represented by CCdl054, CCdl672, CCdl675, MCF7, and T47D.</p>", "links"=>[], "tags"=>["dimensional", "cells", "cancer"], "article_id"=>312109, "categories"=>["Biological Sciences", "Biotechnology", "Cancer", "Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Ashley A. Powell", "AmirAli H. Talasaz", "Haiyu Zhang", "Marc A. Coram", "Anupama Reddy", "Glenn Deng", "Melinda L. Telli", "Ranjana H. Advani", "Robert W. Carlson", "Joseph A. Mollick", "Shruti Sheth", "Allison W. Kurian", "James M. Ford", "Frank E. Stockdale", "Stephen R. Quake", "R. Fabian Pease", "Michael N. Mindrinos", "Gyan Bhanot", "Shanaz H. Dairkee", "Ronald W. Davis", "Stefanie S. Jeffrey"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0033788.g003", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_High_dimensional_analysis_of_single_cells_from_breast_cancer_cell_lines_/312109", "title"=>"High dimensional analysis of single cells from breast cancer cell lines.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-07 00:35:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/641977"], "description"=>"<p>Heatmap of single cell gene expression for 31-gene subset data derived from seven breast cancer cell lines and 105 CTCs isolated from patients with primary and metastatic breast cancer. Yellow indicates high gene expression; gray is median expression; blue indicates low expression; and black represents undetectable expression. The samples reveal two robust clusters for CTCs (lavender: Cluster I; turquoise blue: Cluster II) and two clusters representing primary (pink: CCdl054, orange: CCdl672, gold: CCdl675) and metastatic cell lines. Note dendrogram branches that cluster ER-negative cell lines (red: MDA-231; plum: SKBR3) and ER-positive cell lines (dark green: MCF7, and bright green: T47D).</p>", "links"=>[], "tags"=>["cancer", "ctc"], "article_id"=>312437, "categories"=>["Biological Sciences", "Biotechnology", "Cancer", "Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Ashley A. Powell", "AmirAli H. Talasaz", "Haiyu Zhang", "Marc A. Coram", "Anupama Reddy", "Glenn Deng", "Melinda L. Telli", "Ranjana H. Advani", "Robert W. Carlson", "Joseph A. Mollick", "Shruti Sheth", "Allison W. Kurian", "James M. Ford", "Frank E. Stockdale", "Stephen R. Quake", "R. Fabian Pease", "Michael N. Mindrinos", "Gyan Bhanot", "Shanaz H. Dairkee", "Ronald W. Davis", "Stefanie S. Jeffrey"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0033788.g005", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Combined_breast_cancer_cell_line_and_CTC_clusters_/312437", "title"=>"Combined breast cancer cell line and CTC clusters.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-07 00:40:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/642147"], "description"=>"<p>Phenotype of Primary Tumors in CTC Clusters.</p>", "links"=>[], "tags"=>["tumors", "ctc"], "article_id"=>312611, "categories"=>["Biological Sciences", "Biotechnology", "Cancer", "Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Ashley A. Powell", "AmirAli H. Talasaz", "Haiyu Zhang", "Marc A. Coram", "Anupama Reddy", "Glenn Deng", "Melinda L. Telli", "Ranjana H. Advani", "Robert W. Carlson", "Joseph A. Mollick", "Shruti Sheth", "Allison W. Kurian", "James M. Ford", "Frank E. Stockdale", "Stephen R. Quake", "R. Fabian Pease", "Michael N. Mindrinos", "Gyan Bhanot", "Shanaz H. Dairkee", "Ronald W. Davis", "Stefanie S. Jeffrey"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0033788.t001", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phenotype_of_Primary_Tumors_in_CTC_Clusters_/312611", "title"=>"Phenotype of Primary Tumors in CTC Clusters.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-05-07 00:43:31"}
  • {"files"=>["https://ndownloader.figshare.com/files/641384"], "description"=>"<p>A. MagSweeper device showing magnetic rods sheathed in plastic above the capture, wash and release stations. B. A diagrammatic view of MagSweeper cell isolation protocol. C. A controlled shear force produced by the movement of the magnetic rods in the wash station releases non-specifically bound blood cells. For cells with attached magnetic beads (black circles), the magnetic rod produces a magnetic force in z proportion to the nonuniformity (dB2/dz) of the magnetic field, thus imparting momentum in z proportional to (dB2/dz) and to a dwell time that depends both on the sweep speed and on the velocity distribution across the boundary layer that extends into the fluid from the surface of the sheath, optimizing capture of labeled cells and release of contaminating unlabeled cells. D. Photomicrograph (200X) of a CTC labeled with 4.5 µm immunomagnetic beads isolated from a patient with metastatic breast cancer. Magnetic beads are small dark spheres; the CTC appears as a translucent cell surrounded by clusters of beads.</p>", "links"=>[], "tags"=>["genetics and genomics", "molecular biology", "biotechnology", "Computational biology", "cell biology", "oncology"], "article_id"=>311842, "categories"=>["Biological Sciences", "Biotechnology", "Cancer", "Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Ashley A. Powell", "AmirAli H. Talasaz", "Haiyu Zhang", "Marc A. Coram", "Anupama Reddy", "Glenn Deng", "Melinda L. Telli", "Ranjana H. Advani", "Robert W. Carlson", "Joseph A. Mollick", "Shruti Sheth", "Allison W. Kurian", "James M. Ford", "Frank E. Stockdale", "Stephen R. Quake", "R. Fabian Pease", "Michael N. Mindrinos", "Gyan Bhanot", "Shanaz H. Dairkee", "Ronald W. Davis", "Stefanie S. Jeffrey"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0033788.g001", "stats"=>{"downloads"=>1, "page_views"=>36, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_MagSweeper_instrumentation_and_cell_isolation_steps_/311842", "title"=>"MagSweeper instrumentation, and cell isolation steps.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-07 00:30:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/641802"], "description"=>"<p>Heatmap of single cell gene expression for 31-gene subset data derived from 105 CTCs isolated from patients with primary and metastatic breast cancer. Yellow indicates high gene expression; gray is median expression; blue indicates low expression; and black represents undetectable expression. The samples reveal two robust clusters for CTCs (lavender: Cluster I; turquoise blue: Cluster II). In addition to epithelial markers, these genes include pathways associated with EMT, metastasis, and AKT/mTOR signaling.</p>", "links"=>[], "tags"=>["dimensional", "clustering", "ctcs", "patients"], "article_id"=>312267, "categories"=>["Biological Sciences", "Biotechnology", "Cancer", "Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Ashley A. Powell", "AmirAli H. Talasaz", "Haiyu Zhang", "Marc A. Coram", "Anupama Reddy", "Glenn Deng", "Melinda L. Telli", "Ranjana H. Advani", "Robert W. Carlson", "Joseph A. Mollick", "Shruti Sheth", "Allison W. Kurian", "James M. Ford", "Frank E. Stockdale", "Stephen R. Quake", "R. Fabian Pease", "Michael N. Mindrinos", "Gyan Bhanot", "Shanaz H. Dairkee", "Ronald W. Davis", "Stefanie S. Jeffrey"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0033788.g004", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_High_dimensional_single_cell_analysis_and_clustering_of_CTCs_isolated_from_patients_with_breast_cancer_/312267", "title"=>"High dimensional single cell analysis and clustering of CTCs isolated from patients with breast cancer.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-07 00:37:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/641520"], "description"=>"<p>A. Gene expression heat maps of C<sub>T</sub> measurements of 15 genes by microfluidic qRT-PCR assays performed on single MCF7 cells before and after labeling and capture by the MagSweeper. Each gene is measured in triplicate for each single cell. Some single cell expression variation is inherent among individual cells, but the overall pattern showed no marked effect by our isolation protocol. B. Average plating efficiency (percent of single cells that formed colonies after seven days) of MCF7 cells; either control, labeled with beads, or labeled and captured by the MagSweeper, performed in triplicate. This demonstrates that cell viability was not affected by our purification protocol.</p>", "links"=>[], "tags"=>["viability", "magsweeper"], "article_id"=>311986, "categories"=>["Biological Sciences", "Biotechnology", "Cancer", "Molecular Biology", "Cell Biology", "Genetics"], "users"=>["Ashley A. Powell", "AmirAli H. Talasaz", "Haiyu Zhang", "Marc A. Coram", "Anupama Reddy", "Glenn Deng", "Melinda L. Telli", "Ranjana H. Advani", "Robert W. Carlson", "Joseph A. Mollick", "Shruti Sheth", "Allison W. Kurian", "James M. Ford", "Frank E. Stockdale", "Stephen R. Quake", "R. Fabian Pease", "Michael N. Mindrinos", "Gyan Bhanot", "Shanaz H. Dairkee", "Ronald W. Davis", "Stefanie S. Jeffrey"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0033788.g002", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Unperturbed_gene_expression_and_cell_viability_of_MagSweeper_isolated_tumor_cells_/311986", "title"=>"Unperturbed gene expression and cell viability of MagSweeper isolated tumor cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-07 00:33:06"}

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