Redifferentiation of Adult Human β Cells Expanded In Vitro by Inhibition of the WNT Pathway
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{"title"=>"Redifferentiation of adult human β cells expanded in vitro by inhibition of the WNT pathway", "type"=>"journal", "authors"=>[{"first_name"=>"Ayelet", "last_name"=>"Lenz", "scopus_author_id"=>"53982813000"}, {"first_name"=>"Ginat", "last_name"=>"Toren-Haritan", "scopus_author_id"=>"36186045900"}, {"first_name"=>"Shimon", "last_name"=>"Efrat", "scopus_author_id"=>"57193206288"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"25393025", "sgr"=>"84911912000", "doi"=>"10.1371/journal.pone.0112914", "scopus"=>"2-s2.0-84911912000", "pui"=>"600506786", "issn"=>"19326203"}, "id"=>"fa4234b6-3991-3672-a9ee-2ed357b7a532", "abstract"=>"In vitro expansion of adult human islet β cells is an attractive solution for the shortage of tissue for cell replacement therapy of type 1 diabetes. Using a lineage tracing approach we have demonstrated that β-cell-derived (BCD) cells rapidly dedifferentiate in culture and can proliferate for up to 16 population doublings. Dedifferentiation is associated with changes resembling epithelial-mesenchymal transition (EMT). The WNT pathway has been shown to induce EMT and plays key roles in regulating replication and differentiation in many cell types. Here we show that BCD cell dedifferentiation is associated with β-catenin translocation into the nucleus and activation of the WNT pathway. Inhibition of β-catenin expression in expanded BCD cells using short hairpin RNA resulted in growth arrest, mesenchymal-epithelial transition, and redifferentiation, as judged by activation of β-cell gene expression. Furthermore, inhibition of β-catenin expression synergized with redifferentiation induced by a combination of soluble factors, as judged by an increase in the number of C-peptide-positive cells. Simultaneous inhibition of the WNT and NOTCH pathways also resulted in a synergistic effect on redifferentiation. These findings, which were reproducible in cells derived from multiple human donors, suggest that inhibition of the WNT pathway may contribute to a therapeutically applicable way for generation of functional insulin-producing cells following ex-vivo expansion.", "link"=>"http://www.mendeley.com/research/redifferentiation-adult-human-%CE%B2-cells-expanded-vitro-inhibition-wnt-pathway", "reader_count"=>16, "reader_count_by_academic_status"=>{"Researcher"=>6, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>4, "Student > Master"=>3, "Professor"=>1}, "reader_count_by_user_role"=>{"Researcher"=>6, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>4, "Student > Master"=>3, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>4, "Agricultural and Biological Sciences"=>7, "Medicine and Dentistry"=>3, "Pharmacology, Toxicology and Pharmaceutical Science"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>7}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Unspecified"=>{"Unspecified"=>1}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"Japan"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1793258"], "description"=>"<p>Primer sequences for qPCR analyses.</p>", "links"=>[], "tags"=>["notch", "emt", "16 population doublings", "rna", "cell replacement therapy", "Type 1 diabetes", "WNT pathway", "Adult Human β Cells", "BCD cell dedifferentiation"], "article_id"=>1240589, "categories"=>["Biological Sciences"], "users"=>["Ayelet Lenz", "Ginat Toren-Haritan", "Shimon Efrat"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0112914.t002", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Primer_sequences_for_qPCR_analyses_/1240589", "title"=>"Primer sequences for qPCR analyses.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-11-13 03:51:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/1793240"], "description"=>"<p><b>A</b>, qPCR analysis of RNA extracted from isolated islets (p0) and expanded islet cells at the indicated passage number. Data are mean±SE (n = 4 donors). *p<0.05, relative to p0. <b>B</b>, qPCR analysis of RNA extracted from sorted eGFP<sup>+</sup> BCD cells at passages 6–8, 7 days following infection with β-catenin or NT shRNA viruses. Data are mean±SE (n = 3 donors). *p<0.05, relative to NT shRNA. <b>C,D</b>, Immunoblotting of FOXO1 and phospho-FOXO1 in expanded islet cells infected at passages 5–6 with β-catenin or NT shRNA viruses, and analyzed 7 days later. Data are mean±SE (n = 4 donors). *p<0.05, relative to NT shRNA. <b>E</b>, Proposed mechanism for activation of insulin transcription by β-catenin downregulation.</p>", "links"=>[], "tags"=>["notch", "emt", "16 population doublings", "rna", "cell replacement therapy", "Type 1 diabetes", "WNT pathway", "Adult Human β Cells", "BCD cell dedifferentiation"], "article_id"=>1240574, "categories"=>["Biological Sciences"], "users"=>["Ayelet Lenz", "Ginat Toren-Haritan", "Shimon Efrat"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0112914.g006", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_946_catenin_downregulation_on_expression_of_AKT1_and_FOXO1_/1240574", "title"=>"Effect of β-catenin downregulation on expression of AKT1 and FOXO1.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-11-13 03:51:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/1793237"], "description"=>"<p><b>A</b>, Heat map of cDNA microarray analysis of RNA extracted from sorted eGFP<sup>+</sup> BCD cells at passages 4–5, 7 days following infection with β-catenin or NT shRNA viruses. n = 4 donors for β-catenin shRNA; n = 3 donors for NT shRNA. <b>B</b>, Gene ontology analysis of cDNA microarray results. <b>C</b>, Validation of candidate genes from the microarray analysis by qPCR analysis of RNA extracted from eGFP<sup>+</sup> BCD cells at passages 5–6, 7 days following infection with β-catenin or NT shRNA viruses. Data are mean±SE (n = 3–4 donors). *p<0.05, **p<0.005, relative to NT shRNA. Validation of IAPP transcripts is seen in D.</p>", "links"=>[], "tags"=>["notch", "emt", "16 population doublings", "rna", "cell replacement therapy", "Type 1 diabetes", "WNT pathway", "Adult Human β Cells", "BCD cell dedifferentiation"], "article_id"=>1240571, "categories"=>["Biological Sciences"], "users"=>["Ayelet Lenz", "Ginat Toren-Haritan", "Shimon Efrat"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0112914.g005", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Global_changes_in_gene_expression_in_BCD_cells_infected_with_946_catenin_shRNA_/1240571", "title"=>"Global changes in gene expression in BCD cells infected with β-catenin shRNA.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-11-13 03:51:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/1793222"], "description"=>"<p><b>A</b>,<b>B</b>, Immunoblotting of β-catenin in expanded islet cells infected at passage 5 with β-catenin or nontarget (NT) shRNA viruses. HSC70 was used as a loading control. Data are mean±SE (n = 3 donors), shown as percentage of untreated (UTR) cells. *p<0.005, compared with NT shRNA. <b>C</b>. Immunofluorescence of Ki67 in expanded islet cells infected at passages 5–6 with β-catenin or NT shRNA viruses, and analyzed 7 days later. Values are mean±SD (n = 3 donors), based on counting >1000 cells per donor. **p<0.005, relative NT shRNA. Bar = 50 µm. <b>D</b>, qPCR analysis of RNA extracted from expanded islet cells at passages 5–6, 7 days following infection with β-catenin or NT shRNA viruses. Data are mean±SE (n = 3–4 donors). * p<0.05, relative to NT shRNA. Values on top of bars indicate fold change relative to NT shRNA.</p>", "links"=>[], "tags"=>["notch", "emt", "16 population doublings", "rna", "cell replacement therapy", "Type 1 diabetes", "WNT pathway", "Adult Human β Cells", "BCD cell dedifferentiation"], "article_id"=>1240556, "categories"=>["Biological Sciences"], "users"=>["Ayelet Lenz", "Ginat Toren-Haritan", "Shimon Efrat"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0112914.g002", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_946_catenin_downregulation_on_islet_cell_proliferation_/1240556", "title"=>"Effect of β-catenin downregulation on islet cell proliferation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-11-13 03:51:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/1793251"], "description"=>"<p><b>A</b>, Effect of a 4-day RC treatment on levels of WNT pathway gene transcripts in expanded islet cells at passages 5–6. Data are mean±SE (n = 4–5 donors). *p<0.05, compared with UTR cells. <b>B</b>, Effect of a 4-day RC treatment on subcellular localization of β-catenin in expanded islet cells at passage 6. Beta-catenin is localized throughout the cell in >98% of expanded untreated cells, while >98% of cells treated with β-catenin shRNA show β-catenin membrane localization. Bar = 50 µm. <b>C</b>, Effect of a 4-day RC treatment on levels of WNT pathway gene transcripts in sorted eGFP<sup>+</sup> BCD cells at passages 5–6. Data are mean±SE (n = 3–4 donors). *p<0.05, compared with UTR cells. <b>D</b>,<b>E</b>, Synergistic effect of a 8-day RC treatment and β-catenin shRNA on levels of WNT pathway target gene (D) and β-cell transcripts (E) in expanded islet cells at passages 5–6. Data are mean±SE (n = 3–5 donors). *p<0.05, relative to nontarget shRNA. <b>F</b>, C-peptide immunofluorescence in expanded islet cells infected at passages 5–6 with β-catenin or NT shRNA viruses, and treated for 4 days with RC. Bar = 75 µm. Values are mean±SD (n = 3 donors), based on quantitation of >1000 cells in each group. *p<0.005, relative NT shRNA.</p>", "links"=>[], "tags"=>["notch", "emt", "16 population doublings", "rna", "cell replacement therapy", "Type 1 diabetes", "WNT pathway", "Adult Human β Cells", "BCD cell dedifferentiation"], "article_id"=>1240582, "categories"=>["Biological Sciences"], "users"=>["Ayelet Lenz", "Ginat Toren-Haritan", "Shimon Efrat"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0112914.g007", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Synergistic_effects_of_946_catenin_downregulation_and_RC_treatment_/1240582", "title"=>"Synergistic effects of β-catenin downregulation and RC treatment.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-11-13 03:51:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/1793262", "https://ndownloader.figshare.com/files/1793263"], "description"=>"<div><p>In vitro expansion of adult human islet β cells is an attractive solution for the shortage of tissue for cell replacement therapy of type 1 diabetes. Using a lineage tracing approach we have demonstrated that β-cell-derived (BCD) cells rapidly dedifferentiate in culture and can proliferate for up to 16 population doublings. Dedifferentiation is associated with changes resembling epithelial-mesenchymal transition (EMT). The WNT pathway has been shown to induce EMT and plays key roles in regulating replication and differentiation in many cell types. Here we show that BCD cell dedifferentiation is associated with β-catenin translocation into the nucleus and activation of the WNT pathway. Inhibition of β-catenin expression in expanded BCD cells using short hairpin RNA resulted in growth arrest, mesenchymal-epithelial transition, and redifferentiation, as judged by activation of β-cell gene expression. Furthermore, inhibition of β-catenin expression synergized with redifferentiation induced by a combination of soluble factors, as judged by an increase in the number of C-peptide-positive cells. Simultaneous inhibition of the WNT and NOTCH pathways also resulted in a synergistic effect on redifferentiation. These findings, which were reproducible in cells derived from multiple human donors, suggest that inhibition of the WNT pathway may contribute to a therapeutically applicable way for generation of functional insulin-producing cells following ex-vivo expansion.</p></div>", "links"=>[], "tags"=>["notch", "emt", "16 population doublings", "rna", "cell replacement therapy", "Type 1 diabetes", "WNT pathway", "Adult Human β Cells", "BCD cell dedifferentiation"], "article_id"=>1240593, "categories"=>["Biological Sciences"], "users"=>["Ayelet Lenz", "Ginat Toren-Haritan", "Shimon Efrat"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0112914.s001", "https://dx.doi.org/10.1371/journal.pone.0112914.s002"], "stats"=>{"downloads"=>4, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Redifferentiation_of_Adult_Human_Cells_Expanded_In_Vitro_by_Inhibition_of_the_WNT_Pathway/1240593", "title"=>"Redifferentiation of Adult Human β Cells Expanded <i>In Vitro</i> by Inhibition of the WNT Pathway", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-11-13 03:51:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/1793207"], "description"=>"<p><b>A</b>, qPCR analysis of RNA extracted from isolated islets (p0) and expanded islet cells at the indicated passage number. <b>B</b>, qPCR analysis of RNA extracted from sorted eGFP<sup>+</sup> BCD cells at passages 5–6. Data in A and C are mean±SE (n = 3–5 donors). *p<0.05, **p<0.005, compared with P0. <b>C</b>, Immunofluorescence analysis of isolated islets, and expanded islet cells at passage 6. Beta-catenin is localized in the membrane region in >98% of islet cells, while >98% of cells at passage 6 show β-catenin nuclear localization. Active β-catenin was not detected in islet β cells. Bar = 50 µm.</p>", "links"=>[], "tags"=>["notch", "emt", "16 population doublings", "rna", "cell replacement therapy", "Type 1 diabetes", "WNT pathway", "Adult Human β Cells", "BCD cell dedifferentiation"], "article_id"=>1240541, "categories"=>["Biological Sciences"], "users"=>["Ayelet Lenz", "Ginat Toren-Haritan", "Shimon Efrat"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0112914.g001", "stats"=>{"downloads"=>2, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Upregulation_of_the_WNT_pathway_in_BCD_cells_/1240541", "title"=>"Upregulation of the WNT pathway in BCD cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-11-13 03:51:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/1793259"], "description"=>"<p>Genes selected for validation of microarray results by qPCR.</p>", "links"=>[], "tags"=>["notch", "emt", "16 population doublings", "rna", "cell replacement therapy", "Type 1 diabetes", "WNT pathway", "Adult Human β Cells", "BCD cell dedifferentiation"], "article_id"=>1240590, "categories"=>["Biological Sciences"], "users"=>["Ayelet Lenz", "Ginat Toren-Haritan", "Shimon Efrat"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0112914.t003", "stats"=>{"downloads"=>2, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genes_selected_for_validation_of_microarray_results_by_qPCR_/1240590", "title"=>"Genes selected for validation of microarray results by qPCR.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-11-13 03:51:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/1793256"], "description"=>"<p>Donors of islets used in the study.</p>", "links"=>[], "tags"=>["notch", "emt", "16 population doublings", "rna", "cell replacement therapy", "Type 1 diabetes", "WNT pathway", "Adult Human β Cells", "BCD cell dedifferentiation"], "article_id"=>1240587, "categories"=>["Biological Sciences"], "users"=>["Ayelet Lenz", "Ginat Toren-Haritan", "Shimon Efrat"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0112914.t001", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Donors_of_islets_used_in_the_study_/1240587", "title"=>"Donors of islets used in the study.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-11-13 03:51:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/1793255"], "description"=>"<p><b>A</b>, qPCR analysis of RNA extracted from expanded islet cells at passage 6, 7 days following infection with β-catenin shRNA, HES1 shRNA, or both. Data are mean±SE (n = 3 donors). *p<0.05, **p<0.005. <b>B</b>, Effect of β-catenin downregulation on levels of NOTCH pathway gene transcripts. qPCR analysis of RNA extracted from expanded islet cells at passages 5–6, 7 days following infection with β-catenin or NT shRNA viruses. Data are mean±SE (n = 3–8 donors). *p<0.05, **p<0.005, relative to NT shRNA.</p>", "links"=>[], "tags"=>["notch", "emt", "16 population doublings", "rna", "cell replacement therapy", "Type 1 diabetes", "WNT pathway", "Adult Human β Cells", "BCD cell dedifferentiation"], "article_id"=>1240586, "categories"=>["Biological Sciences"], "users"=>["Ayelet Lenz", "Ginat Toren-Haritan", "Shimon Efrat"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0112914.g008", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Synegistic_effects_of_946_catenin_and_HES1_downregulation_/1240586", "title"=>"Synegistic effects of β-catenin and HES1 downregulation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-11-13 03:51:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/1793233"], "description"=>"<p><b>A</b>, qPCR analysis of RNA extracted from expanded islet cells at passages 4–5, 7 days following infection with increasing amounts of β-catenin or NT shRNA viruses. Data are mean±SE (n = 3 donors). *p<0.05, **p<0.005, relative to NT shRNA. <b>B</b>, qPCR analysis of RNA extracted from expanded islet cells at passages 5–7, 7 days following infection with β-catenin or NT shRNA viruses. Data are mean±SE (n = 3–8 donors). *p<0.05, **p<0.005, relative NT shRNA. <b>C</b>, C-peptide immunofluorescence in expanded islet cells infected at passages 5–7 with β-catenin or NT shRNA viruses, and analyzed 7 days later. Bar = 50 µm Values are mean±SD (n = 4 donors), based on quantitation of >1000 cells in each group. *p<0.005, relative NT shRNA. <b>D</b>, qPCR analysis of RNA extracted from sorted eGFP<sup>+</sup> BCD cells at passages 6–8, 7 days following infection with β-catenin or NT shRNA viruses. Data are mean±SE (n = 3–4 donors). *p<0.05, relative to NT shRNA.</p>", "links"=>[], "tags"=>["notch", "emt", "16 population doublings", "rna", "cell replacement therapy", "Type 1 diabetes", "WNT pathway", "Adult Human β Cells", "BCD cell dedifferentiation"], "article_id"=>1240567, "categories"=>["Biological Sciences"], "users"=>["Ayelet Lenz", "Ginat Toren-Haritan", "Shimon Efrat"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0112914.g004", "stats"=>{"downloads"=>4, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_946_catenin_downregulation_on_BCD_cell_redifferentiation_/1240567", "title"=>"Effect of β-catenin downregulation on BCD cell redifferentiation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-11-13 03:51:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/1793228"], "description"=>"<p><b>A</b>,<b>B</b>, qPCR analysis of RNA extracted from expanded islet cells at passages 5–6, 7 days following infection with β-catenin or NT shRNA viruses. Data are mean±SE (n = 3–4 donors). * p<0.05, ** p<0.005, relative to NT shRNA. <b>C</b>,<b>D</b>, Immunoblotting of SNAI2 in expanded islet cells infected at passage 5 with β-catenin or NT shRNA viruses, and analyzed 7 days later. Data are mean±SE (n = 3 donors). *p<0.05.</p>", "links"=>[], "tags"=>["notch", "emt", "16 population doublings", "rna", "cell replacement therapy", "Type 1 diabetes", "WNT pathway", "Adult Human β Cells", "BCD cell dedifferentiation"], "article_id"=>1240562, "categories"=>["Biological Sciences"], "users"=>["Ayelet Lenz", "Ginat Toren-Haritan", "Shimon Efrat"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0112914.g003", "stats"=>{"downloads"=>3, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_946_catenin_downregulation_on_EMT_marker_gene_expression_in_expanded_islet_cells_/1240562", "title"=>"Effect of β-catenin downregulation on EMT marker gene expression in expanded islet cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-11-13 03:51:55"}

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Relative Metric

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