Combined Flow Cytometric Analysis of Surface and Intracellular Antigens Reveals Surface Molecule Markers of Human Neuropoiesis
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{"title"=>"Combined Flow Cytometric Analysis of Surface and Intracellular Antigens Reveals Surface Molecule Markers of Human Neuropoiesis", "type"=>"journal", "authors"=>[{"first_name"=>"Gizem", "last_name"=>"Turaç", "scopus_author_id"=>"55775961600"}, {"first_name"=>"Christopher J.", "last_name"=>"Hindley", "scopus_author_id"=>"26967798500"}, {"first_name"=>"Ria", "last_name"=>"Thomas", "scopus_author_id"=>"55776822700"}, {"first_name"=>"Jason A.", "last_name"=>"Davis", "scopus_author_id"=>"57199369779"}, {"first_name"=>"Michela", "last_name"=>"Deleidi", "scopus_author_id"=>"8613948600"}, {"first_name"=>"Thomas", "last_name"=>"Gasser", "scopus_author_id"=>"35519668300"}, {"first_name"=>"Erdal", "last_name"=>"Karaöz", "scopus_author_id"=>"7003448087"}, {"first_name"=>"Jan", "last_name"=>"Pruszak", "scopus_author_id"=>"8617335100"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "pui"=>"369200061", "doi"=>"10.1371/journal.pone.0068519", "sgr"=>"84879486703", "scopus"=>"2-s2.0-84879486703", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pmid"=>"23826393"}, "id"=>"765737ce-6426-3333-9239-4e119be39a64", "abstract"=>"Surface molecule profiles undergo dynamic changes in physiology and pathology, serve as markers of cellular state and phenotype and can be exploited for cell selection strategies and diagnostics. The isolation of well-defined cell subsets is needed for in vivo and in vitro applications in stem cell biology. In this technical report, we present an approach for defining a subset of interest in a mixed cell population by flow cytometric detection of intracellular antigens. We have developed a fully validated protocol that enables the co-detection of cluster of differentiation (CD) surface antigens on fixed, permeabilized neural cell populations defined by intracellular staining. Determining the degree of co-expression of surface marker candidates with intracellular target population markers (nestin, MAP2, doublecortin, TUJ1) on neuroblastoma cell lines (SH-SY5Y, BE(2)-M17) yielded a combinatorial CD49f(-)/CD200(high) surface marker panel. Its application in fluorescence-activated cell sorting (FACS) generated enriched neuronal cultures from differentiated cell suspensions derived from human induced pluripotent stem cells. Our data underlines the feasibility of using the described co-labeling protocol and co-expression analysis for quantitative assays in mammalian neurobiology and for screening approaches to identify much needed surface markers in stem cell biology.", "link"=>"http://www.mendeley.com/research/combined-flow-cytometric-analysis-surface-intracellular-antigens-reveals-surface-molecule-markers-hu", "reader_count"=>86, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Student > Doctoral Student"=>8, "Researcher"=>15, "Student > Ph. D. Student"=>26, "Student > Postgraduate"=>5, "Student > Master"=>11, "Other"=>8, "Student > Bachelor"=>6, "Lecturer > Senior Lecturer"=>1, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Student > Doctoral Student"=>8, "Researcher"=>15, "Student > Ph. D. Student"=>26, "Student > Postgraduate"=>5, "Student > Master"=>11, "Other"=>8, "Student > Bachelor"=>6, "Lecturer > Senior Lecturer"=>1, "Professor"=>3}, "reader_count_by_subject_area"=>{"Engineering"=>4, "Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>7, "Agricultural and Biological Sciences"=>51, "Medicine and Dentistry"=>10, "Neuroscience"=>8, "Pharmacology, Toxicology and Pharmaceutical Science"=>2, "Immunology and Microbiology"=>2, "Physics and Astronomy"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>4}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>10}, "Neuroscience"=>{"Neuroscience"=>8}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>51}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>7}, "Unspecified"=>{"Unspecified"=>1}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>2}}, "reader_count_by_country"=>{"United States"=>4, "Brazil"=>2, "France"=>2, "Germany"=>1}, "group_count"=>7}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1098636"], "description"=>"<p>CD24 surface antigen detection on SH-SY5Y cells remained largely stable with 4% PFA fixation after staining (<b>A</b>, <b>B</b>), yet was greatly reduced with permeabilization using Triton X-100(C, D). Lowering PFA concentration combined with Tween-20 for permeabilization restored CD24 surface staining to levels approximating those seen on live cells (<b>E</b>, <b>F</b>; see <b>A</b>). Optimizing fixation and permeabilization (<b>H</b> to <b>K</b>) enabled simultaneous detection of intracellular antigens, here TUJ1 (β-III-tubulin) while preserving cell surface staining (see <b>F</b>, <b>K</b>). Panel (<b>G</b>) provides a quantitative overview of the different conditions (i-vi indicating the conditions as labeled in <b>A</b> to <b>F</b>). Incubation of live or solely fixed cells with antibodies targeting intracellular epitopes without permeabilization results in no detection. Representative scatter plots for ≥ three independent experimental repeats are shown.</p>", "links"=>[], "tags"=>["cd", "labeling", "detection", "intracellular"], "article_id"=>729581, "categories"=>["Biological Sciences"], "users"=>["Gizem Turaç", "Christopher J. Hindley", "Ria Thomas", "Jason A. Davis", "Michela Deleidi", "Thomas Gasser", "Erdal Karaöz", "Jan Pruszak"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068519.g002", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Establishing_conditions_that_maintain_CD_surface_marker_labeling_with_detection_of_intracellular_antigens_/729581", "title"=>"Establishing conditions that maintain CD surface marker labeling with detection of intracellular antigens.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-24 02:17:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1098654", "https://ndownloader.figshare.com/files/1098655", "https://ndownloader.figshare.com/files/1098656"], "description"=>"<div><p>Surface molecule profiles undergo dynamic changes in physiology and pathology, serve as markers of cellular state and phenotype and can be exploited for cell selection strategies and diagnostics. The isolation of well-defined cell subsets is needed for <i>in vivo</i> and <i>in vitro</i> applications in stem cell biology. In this technical report, we present an approach for defining a subset of interest in a mixed cell population by flow cytometric detection of intracellular antigens. We have developed a fully validated protocol that enables the co-detection of cluster of differentiation (CD) surface antigens on fixed, permeabilized neural cell populations defined by intracellular staining. Determining the degree of co-expression of surface marker candidates with intracellular target population markers (nestin, MAP2, doublecortin, TUJ1) on neuroblastoma cell lines (SH-SY5Y, BE(2)-M17) yielded a combinatorial CD49f<sup>-</sup>/CD200<sup>high</sup> surface marker panel. Its application in fluorescence-activated cell sorting (FACS) generated enriched neuronal cultures from differentiated cell suspensions derived from human induced pluripotent stem cells. Our data underlines the feasibility of using the described co-labeling protocol and co-expression analysis for quantitative assays in mammalian neurobiology and for screening approaches to identify much needed surface markers in stem cell biology.</p> </div>", "links"=>[], "tags"=>["cytometric", "intracellular", "antigens", "reveals", "markers"], "article_id"=>729588, "categories"=>["Biological Sciences"], "users"=>["Gizem Turaç", "Christopher J. Hindley", "Ria Thomas", "Jason A. Davis", "Michela Deleidi", "Thomas Gasser", "Erdal Karaöz", "Jan Pruszak"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0068519.s001", "https://dx.doi.org/10.1371/journal.pone.0068519.s002", "https://dx.doi.org/10.1371/journal.pone.0068519.s003"], "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Combined_Flow_Cytometric_Analysis_of_Surface_and_Intracellular_Antigens_Reveals_Surface_Molecule_Markers_of_Human_Neuropoiesis_/729588", "title"=>"Combined Flow Cytometric Analysis of Surface and Intracellular Antigens Reveals Surface Molecule Markers of Human Neuropoiesis", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-06-24 02:17:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1098645"], "description"=>"<p>(<b>A</b>) In SH-SY5Y cells CD49f, CD90<sup>HIGH</sup> and CD29 expression clustered distinct from doublecortin (DCX)-positivity, while subsets of CD56, CD24 and CD200 closely correlated with neuronal differentiation (DCX+). Patterns of exclusive positivity on either the y- or the x-axis (upper left and lower right quadrant) yield CD marker candidates for negative selection strategies. Patterns of shared intracellular and surface expression (upper right quadrant) are suitable for positive selection strategies. Blue outlines illustrate co-expression patterns. (<b>B</b>) Co-localization analysis of the catecholaminergic intracellular marker tyrosine hydroxylase (TH) is shown on BE(2)-M17 cells. The TH-positive subset stained negative for the putative proliferative indicator CD49f but was colocalized with CD90, CD24 and CD200 in this cell line. (<b>C</b>) Co-localization analysis of the glial intracellular marker glial fibrillary acidic protein (GFAP) is shown on SNB-19 cells. In contrast to the other neural cell lines analyzed, GFAP-positive subsets stained positive for CD49f, and also CD90. CD24 was present to a lower degree and the putative neuronal marker CD200 in this context was virtually absent.</p>", "links"=>[], "tags"=>["detection", "neural", "intracellular", "markers", "antigens"], "article_id"=>729585, "categories"=>["Biological Sciences"], "users"=>["Gizem Turaç", "Christopher J. Hindley", "Ria Thomas", "Jason A. Davis", "Michela Deleidi", "Thomas Gasser", "Erdal Karaöz", "Jan Pruszak"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068519.g006", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Combinatorial_detection_of_known_neural_intracellular_markers_plus_a_panel_of_candidate_surface_antigens_in_human_cell_lines_/729585", "title"=>"Combinatorial detection of known neural intracellular markers plus a panel of candidate surface antigens in human cell lines.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-24 02:17:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1098641"], "description"=>"<p>The detailed list of steps illustrates the working protocol for combined surface and intracellular epitope staining of mammalian cells for flow cytometric analysis. See methods section for further details on reagents and procedures.</p>", "links"=>[], "tags"=>[], "article_id"=>729583, "categories"=>["Biological Sciences"], "users"=>["Gizem Turaç", "Christopher J. Hindley", "Ria Thomas", "Jason A. Davis", "Michela Deleidi", "Thomas Gasser", "Erdal Karaöz", "Jan Pruszak"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068519.g004", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Optimized_protocol_/729583", "title"=>"Optimized protocol.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-24 02:17:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1098643"], "description"=>"<p>(<b>A</b>) Flow cytometry for the intracellular antigens TUJ1, MAP2 and doublecortin (DCX) analyzed on various cell sources including neuroblastoma BE(2)-M17 and SH-SY5Y as well as human iPS cell-derived differentiated neural stem cell cultures (hiPS-NSC). Grey boxes in flow cytometry plots specify gates set on negative control samples to capture 0.4%. Green boxes specify positive fraction on stained samples. Error bars in (<b>B</b>) indicate standard deviation.</p>", "links"=>[], "tags"=>["quantitative", "intracellular", "markers", "neural"], "article_id"=>729584, "categories"=>["Biological Sciences"], "users"=>["Gizem Turaç", "Christopher J. Hindley", "Ria Thomas", "Jason A. Davis", "Michela Deleidi", "Thomas Gasser", "Erdal Karaöz", "Jan Pruszak"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068519.g005", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Qualitative_and_quantitative_comparison_of_intracellular_markers_expressed_by_neural_cells_/729584", "title"=>"Qualitative and quantitative comparison of intracellular markers expressed by neural cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-24 02:17:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1098639"], "description"=>"<p>Flow cytometric detection of TUJ1, MAP2 and nestin antigens in BJ fibroblasts and the neural SH-SY5Y cell line (A). TUJ1 and nestin are present in both cell lines, while the mature neuronal marker MAP2 was only detected in SH-SY5Y cells (arrows). Note stable fluorescent levels of the negative population, indicating low background staining using this protocol. Representative experiment of three independent repeats shown. (<b>B</b>) Corresponding validation by immunofluorescence analysis. (<b>C</b>) Quantitation of TUJ1, MAP2 and nestin intracellular antigen detection (n=3). Error bars indicate standard deviation. (<b>D</b>) Response of TUJ1 and MAP2 intracellular antigen expression to 6 DIV of 10 µM retinoic acid (RA) treatment of SH-SY5Y cells. Note disappearance/reduction of subsets negative for these markers (upward shift, green arrows), as well as a shift toward CD184<sup>low</sup> expression with differentiation (blue arrows).</p>", "links"=>[], "tags"=>["detection", "intracellular", "antigens", "optimized", "fixation-permeabilization", "preserving"], "article_id"=>729582, "categories"=>["Biological Sciences"], "users"=>["Gizem Turaç", "Christopher J. Hindley", "Ria Thomas", "Jason A. Davis", "Michela Deleidi", "Thomas Gasser", "Erdal Karaöz", "Jan Pruszak"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068519.g003", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Accurate_detection_of_intracellular_antigens_with_optimized_fixation_permeabilization_conditions_preserving_surface_antigens_/729582", "title"=>"Accurate detection of intracellular antigens with optimized fixation-permeabilization conditions preserving surface antigens.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-24 02:17:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1098634"], "description"=>"<p>Schematic illustrating the research strategy of identifying novel surface marker combinations on a target population in neural and other stem cell differentiation systems for which intracellular, standard immunocytochemical markers are well established. Following harvesting, the resulting single cell suspension is subject to surface antigen candidate staining, followed by gentle fixation, permeabilization and subsequent co-staining with known intracellular markers. CD markers co-labeling the target population serve as positive markers, those absent on the target population serve as negative markers. In a separate, subsequent step, a combination of the identified positive and/or negative CD markers enables the flow cytometric enrichment of the viable population of interest from a heterogeneous cell suspension for further study and biomedical applications.</p>", "links"=>[], "tags"=>[], "article_id"=>729579, "categories"=>["Biological Sciences"], "users"=>["Gizem Turaç", "Christopher J. Hindley", "Ria Thomas", "Jason A. Davis", "Michela Deleidi", "Thomas Gasser", "Erdal Karaöz", "Jan Pruszak"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068519.g001", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Experimental_outline_/729579", "title"=>"Experimental outline.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-24 02:17:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1098651"], "description"=>"<p>(<b>A</b>) Flow cytometric analysis of the intracellular neuronal subpopulation marker tyrosine hydroxylase (TH) with surface marker candidates CD49f and CD200 (on fixed and permeabilized hiPS-NSC). (<b>B</b>, <b>C</b>) Co-expression analysis of CD49f and CD200 with the established neural marker CD24. (<b>D</b>) Co-expression analysis of CD49f with CD71, CD184, CD90, CD200 antigens. Note occurrence of CD49f-negative subset with CD200 co-labeling (green rectangular gate). (<b>E</b>) Presence of CD49f/CD200 subpopulations in hiPS-NSC differentiation (four independent experimental lines). (<b>F</b>) Phase contrast and immunofluorescence imaging post-FACS; hiPS-NSC at 2 hours, DIV 4 and 5 after CD49f/CD200 FACS. [Scale bars: 50µm. Panels <b>B</b> to <b>D</b> on live hiPS-NSC suspensions without fixation and permeabilization].</p>", "links"=>[], "tags"=>["neural", "ips"], "article_id"=>729587, "categories"=>["Biological Sciences"], "users"=>["Gizem Turaç", "Christopher J. Hindley", "Ria Thomas", "Jason A. Davis", "Michela Deleidi", "Thomas Gasser", "Erdal Karaöz", "Jan Pruszak"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068519.g008", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Application_for_neural_cell_isolation_in_human_iPS_cells_/729587", "title"=>"Application for neural cell isolation in human iPS cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-24 02:17:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1098648"], "description"=>"<p>(<b>A</b>) Mixed SH-SY5Y/SNB-19 neuro-glial cell suspensions (without fixation and permeabilization) analyzed by flow cytometry for CD49f-PE and CD200-APC. Polygon gates within the left dot plot indicate selection of CD49f<sup>+</sup>/CD200<sup>-</sup> (red) versus CD49f <sup>-</sup>/CD200<sup>HIGH</sup> (green) populations. (<b>B</b>) Corresponding microscopic analysis of unsorted (left panel) vs. sorted conditions (mid and right panels) 1 div post-sort. Arrows indicate SH-SY5Y cells, arrowhead SNB-19 [phase contrast; scale bars: 50µm]. (<b>C</b>) Immunofluorescence for GFAP (red) and doublecortin (green) of surface marker code-based cell suspensions. Left panel: unsorted; mid panel: CD49f<sup>+</sup>/CD200<sup>-</sup> population post-sort; right panel: CD49f <sup>-</sup>/CD200<sup>HIGH</sup> population. [1 div post-FACS; scale bars: 20µm].</p>", "links"=>[], "tags"=>["neural", "cancer"], "article_id"=>729586, "categories"=>["Biological Sciences"], "users"=>["Gizem Turaç", "Christopher J. Hindley", "Ria Thomas", "Jason A. Davis", "Michela Deleidi", "Thomas Gasser", "Erdal Karaöz", "Jan Pruszak"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068519.g007", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Application_for_neural_cell_isolation_in_human_neural_cancer_lines_/729586", "title"=>"Application for neural cell isolation in human neural cancer lines.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-24 02:17:36"}

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  • {"unique-ip"=>"77", "full-text"=>"79", "pdf"=>"14", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"81", "full-text"=>"99", "pdf"=>"10", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"19", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"71", "full-text"=>"79", "pdf"=>"15", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"8", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}

Relative Metric

{"start_date"=>"2013-01-01T00:00:00Z", "end_date"=>"2013-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences", "average_usage"=>[269, 466, 588, 697, 800, 896, 988, 1076, 1165, 1254, 1340, 1417]}, {"subject_area"=>"/Biology and life sciences/Neuroscience", "average_usage"=>[261, 444, 554, 655, 748, 834, 923, 1004, 1089, 1170, 1244, 1315, 1380]}]}
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