Pdx1 and Ngn3 Overexpression Enhances Pancreatic Differentiation of Mouse ES Cell-Derived Endoderm Population
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{"title"=>"Pdx1 and Ngn3 overexpression enhances pancreatic differentiation of mouse ES cell-derived endoderm population", "type"=>"journal", "authors"=>[{"first_name"=>"Atsushi", "last_name"=>"Kubo", "scopus_author_id"=>"55628552228"}, {"first_name"=>"Robert", "last_name"=>"Stull", "scopus_author_id"=>"57201536231"}, {"first_name"=>"Mitsuaki", "last_name"=>"Takeuchi", "scopus_author_id"=>"35742242600"}, {"first_name"=>"Kristina", "last_name"=>"Bonham", "scopus_author_id"=>"24330907500"}, {"first_name"=>"Valerie", "last_name"=>"Gouon-Evans", "scopus_author_id"=>"6506536540"}, {"first_name"=>"Masayuki", "last_name"=>"Sho", "scopus_author_id"=>"55863591500"}, {"first_name"=>"Masayuki", "last_name"=>"Iwano", "scopus_author_id"=>"7006416389"}, {"first_name"=>"Yoshihiko", "last_name"=>"Saito", "scopus_author_id"=>"35374553000"}, {"first_name"=>"Gordon", "last_name"=>"Keller", "scopus_author_id"=>"35427735700"}, {"first_name"=>"Ralph", "last_name"=>"Snodgrass", "scopus_author_id"=>"7006511328"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"sgr"=>"80052736706", "doi"=>"10.1371/journal.pone.0024058", "pui"=>"362552312", "pmid"=>"21931641", "scopus"=>"2-s2.0-80052736706", "issn"=>"19326203", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "arxiv"=>"physics.ins-det/1105.0298"}, "id"=>"f07bd627-dbab-3d02-b532-bb7724516539", "abstract"=>"In order to define the molecular mechanisms regulating the specification and differentiation of pancreatic β-islet cells, we investigated the effect of upregulating Pdx1 and Ngn3 during the differentiation of the β-islet-like cells from murine embryonic stem (ES) cell-derived activin induced-endoderm. Induced overexpression of Pdx1 resulted in a significant upregulation of insulin (Ins1 and Ins2), and other pancreas-related genes. To enhance the developmental progression from the pancreatic bud to the formation of the endocrine lineages, we induced the overexpression express of Ngn3 together with Pdx1. This combination dramatically increased the level and timing of maximal Ins1 mRNA expression to approximately 100% of that found in the βTC6 insulinoma cell line. Insulin protein and C-peptide expression was confirmed by immunohistochemistry staining. These inductive effects were restricted to c-kit(+) endoderm enriched EB-derived populations suggesting that Pdx1/Ngn3 functions after the specification of pancreatic endoderm. Although insulin secretion was stimulated by various insulin secretagogues, these cells had only limited glucose response. Microarray analysis was used to evaluate the expression of a broad spectrum of pancreatic endocrine cell-related genes as well as genes associated with glucose responses. Taken together, these findings demonstrate the utility of manipulating Pdx1 and Ngn3 expression in a stage-specific manner as an important new strategy for the efficient generation of functionally immature insulin-producing β-islet cells from ES cells.", "link"=>"http://www.mendeley.com/research/pdx1-ngn3-overexpression-enhances-pancreatic-differentiation-mouse-es-cellderived-endoderm-populatio", "reader_count"=>51, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Researcher"=>12, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>15, "Student > Master"=>11, "Other"=>1, "Student > Bachelor"=>4, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Researcher"=>12, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>15, "Student > Master"=>11, "Other"=>1, "Student > Bachelor"=>4, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>10, "Medicine and Dentistry"=>12, "Agricultural and Biological Sciences"=>26, "Economics, Econometrics and Finance"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>12}, "Economics, Econometrics and Finance"=>{"Economics, Econometrics and Finance"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>26}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>10}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"Argentina"=>1, "United States"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/736686"], "description"=>"<p>Tet-pdx1/ngn3 ES cells were cultured under Protocol #3 for 6 days, with Dox-induction of Pdx1 and Ngn3 expression starting at day 4. A) From day 6 through day 18 EBs were cultured according to Protocol #3 (“IMDM/F12”) or in medium in which the IMDM/F12 was replaced with DMEM (“DMEM”) as indicated (Protocol #4), and <i>Ins1</i> mRNA was quantitated at day 18. B) EBs were cultured according to Protocol #4 for the first 6 days and with Dox-induction of Pdx1 and Ngn3 expression starting at day 4. From day 6 through day 18 various concentrations of B27(−RA) were added as indicated. <i>Ins1</i> mRNA was quantitated at day 18. C) EBs were cultured according to Protocol #4 for 6 days, with Dox-induction of Pdx1 and Ngn3 expression starting at day 4. From day 6 through day 26 the medium was only DMEM with BSA without B27(−RA). <i>Ins1</i> mRNA was quantitated from day 13–26. (D–G) Tet-pdx1/ngn3 ES cells were cultured according to Protocol #4 for 24 days with Dox induction starting at day 4. D) EBs were replated at day 24 and cultured in DMEM (BSA). At day 26, Insulin was visualized with a Cy3-conjugated 2<sup>nd</sup> antibody (red) and C-peptide was visualized with a FITC-conjugated 2nd antibody (green). Nuclei were stained with DAPI (blue). Magnification was with a 400× objective. E) EBs, prepared as in panel D, were trypsinized to make single cell suspensions and cytoplasmic insulin was stained and analyzed by FACS. F) EBs were cultured under Protocol #4 for 6 days, with Dox-induction of Pdx1 and Ngn3 expression starting at day 4. From day 6 through day 18 only one group was supplemented with B27(−RA) (1%) as indicated. On either day 18 or day 26 the media was replaced with fresh DMEM with BSA. Supernatants were harvested after 24 hours, and C-peptide was measured by RIA. The data presented are mean of three independent experiments; the error bars represent the SEM. p<0.05 as compared with 1% B27 at day 18. G) EBs were prepared as described in panel F. On day 26 the media was replaced with HKRB buffer containing either low glucose media (2 mM) or high glucose media (20 mM) with or without tolbutamide. Supernatants were harvested after 1 hour and C-peptide was measured by RIA. The data presented are mean of three independent experiments; the error bars represent the SEM. p<0.05 as compared with low glucose without tolbutamide.</p>", "links"=>[], "tags"=>["improves", "pancreatic", "differentiation", "es"], "article_id"=>407024, "categories"=>["Physiology", "Chemistry", "Cell Biology", "Developmental Biology"], "users"=>["Atsushi Kubo", "Robert Stull", "Mitsuaki Takeuchi", "Kristina Bonham", "Valérie Gouon-Evans", "Masayuki Sho", "Masayuki Iwano", "Yoshihiko Saito", "Gordon Keller", "Ralph Snodgrass"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024058.g006", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_DMEM_media_improves_pancreatic_differentiation_of_mouse_ES_cells_/407024", "title"=>"DMEM media improves pancreatic differentiation of mouse ES cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-13 01:57:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/736525"], "description"=>"<p>Tet-pdx1/ngn3 ES cells were cultured according to Protocol #3. At day 16, EBs were replated on glass bottom dishes coated with Matrigel. Replated EBs were stained with antibodies for the indicated markers of endocrine cells. Insulin was visualized with a Cy3-conjugated 2<sup>nd</sup>–stage fluorescent antibody (red) and other markers were visualized with a FITC-conjugated 2<sup>nd</sup>–stage fluorescent antibody (green). Nuclei were stained with DAPI (blue). Magnification of right panel for C-peptide and insulin was with a 1000× objective. Magnification for the other panels was with a 400× objective.</p>", "links"=>[], "tags"=>["pancreatic", "ebs", "induced", "pdx1"], "article_id"=>406865, "categories"=>["Physiology", "Chemistry", "Cell Biology", "Developmental Biology"], "users"=>["Atsushi Kubo", "Robert Stull", "Mitsuaki Takeuchi", "Kristina Bonham", "Valérie Gouon-Evans", "Masayuki Sho", "Masayuki Iwano", "Yoshihiko Saito", "Gordon Keller", "Ralph Snodgrass"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024058.g005", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Endocrine_protein_expression_in_pancreatic_EBs_induced_by_Pdx1_and_Ngn3_/406865", "title"=>"Endocrine protein expression in pancreatic EBs induced by Pdx1 and Ngn3.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-13 01:54:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/735997"], "description"=>"<p>(A, B) Tet-pdx1 ES cells were cultured according to Protocol #1. Pdx1 expressions were induced with Dox (closed circle, Dox<sup>+</sup>) or without (open square, Dox<sup>−</sup>) for 6 to 20 days. A) Gene expression was analyzed by RT-PCR. B) <i>Ins1</i> mRNA levels were quantified by real time PCR and normalized to 18S mRNA levels. (C, D) EBs were differentiated for 6 days according to Protocol #1 and trypsinized to make single cell suspensions. The cells were electroporated with the pIRES2-EGFP vector and then reaggregated for 2–3 additional days with Dox. C) At day 8 (2 days with Dox), EGFP was evaluated by FACS. D) pIRES2 vectors, constructed to express GFP, Pax4, Nkx6.1 or Ngn3, were electroporated into day 6 EBs and allowed to reaggregate. At day 9, EBs were harvested and gene expression was analyzed by RT-PCR. (E, F) Tet-pdx1/ngn3 ES cells were cultured according to Protocol #1. Pdx1 and Ngn3 expression was induced with Dox (closed circle, Dox<sup>+</sup>) or without (open square, Dox<sup>−</sup>) at day 6 and harvested at the indicated time points. E) <i>Ins1</i> mRNA levels were quantified by real time PCR and normalized to levels in βTC6 as described in the <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0024058#s4\" target=\"_blank\">Methods</a>. F) Gene expression was analyzed by RT-PCR. Note, for the day 6 sample, the cells were exposed to Dox for only 1 hour before the samples were harvested.</p>", "links"=>[], "tags"=>["differentiation", "induced", "pdx1"], "article_id"=>406339, "categories"=>["Physiology", "Chemistry", "Cell Biology", "Developmental Biology"], "users"=>["Atsushi Kubo", "Robert Stull", "Mitsuaki Takeuchi", "Kristina Bonham", "Valérie Gouon-Evans", "Masayuki Sho", "Masayuki Iwano", "Yoshihiko Saito", "Gordon Keller", "Ralph Snodgrass"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024058.g001", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Pancreatic_differentiation_induced_by_Pdx1_and_Ngn3_/406339", "title"=>"Pancreatic differentiation induced by Pdx1 and Ngn3.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-13 01:45:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/736109"], "description"=>"<p>Tet-pdx1/ngn3 ES cells were cultured according to Protocol #2. Pdx1 and Ngn3 were induced with or without Dox starting at day 4, and cells were harvested at the indicated time points. (A–D) insulin and 18S mRNA levels were quantified by real time PCR and normalized to levels seen in βTC6 as described in the <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0024058#s4\" target=\"_blank\">Methods</a>. A) Day 4 EBs were trypsinized and reaggregated with BMP4 (closed circles) or without (open squares). EBs were harvested at day 6 and 9. B) Day 4 EBs were trypsinized and reaggregated with BMP4. At day 6, EBs were replated on gelatin coated dishes and floating EBs were transferred to low-cluster dishes at day 7. Attached monolayer EBs (open bar) and floating EBs (closed bar) were harvested at day 9. (C) Floating EBs were cultured according to Protocol #2, with BMP4, and with Dox (circles) or without Dox (open squares). <i>Ins1</i> (black circles) or <i>Ins2</i> (white circles) mRNA levels were quantified by real time PCR and normalized to levels in βTC6 at the times indicated. (D) CXCR4/c-kit double negative (−/−) or double positive (+/+) cells were isolated by FACS from 4 days EBs, reaggregated for two days, and then replated on gelatin coated plates according to Protocol #2, with BMP4. Floating or attached EBs were harvested at day 9 from the following populations: pre-sorted cells (“Pre”); CXCR4/c-kit double negative (“−/−”); and CXCR4/c-kit double positive (“+/+”). These groups were cultured either as non-adherent EBs (“float”) or as attached monolayer cells (“mono”), as indicated.</p>", "links"=>[], "tags"=>["3d", "non-adherent", "improves"], "article_id"=>406454, "categories"=>["Physiology", "Chemistry", "Cell Biology", "Developmental Biology"], "users"=>["Atsushi Kubo", "Robert Stull", "Mitsuaki Takeuchi", "Kristina Bonham", "Valérie Gouon-Evans", "Masayuki Sho", "Masayuki Iwano", "Yoshihiko Saito", "Gordon Keller", "Ralph Snodgrass"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024058.g002", "stats"=>{"downloads"=>2, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_BMP4_and_3D_non_adherent_culture_improves_Ins1_expression_/406454", "title"=>"BMP4 and 3D non-adherent culture improves <i>Ins1</i> expression.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-13 01:47:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/371445", "https://ndownloader.figshare.com/files/371483", "https://ndownloader.figshare.com/files/371564", "https://ndownloader.figshare.com/files/371638"], "description"=>"<div><p>In order to define the molecular mechanisms regulating the specification and differentiation of pancreatic β-islet cells, we investigated the effect of upregulating Pdx1 and Ngn3 during the differentiation of the β-islet-like cells from murine embryonic stem (ES) cell-derived activin induced-endoderm. Induced overexpression of Pdx1 resulted in a significant upregulation of insulin (<em>Ins1</em> and <em>Ins2</em>), and other pancreas-related genes. To enhance the developmental progression from the pancreatic bud to the formation of the endocrine lineages, we induced the overexpression express of Ngn3 together with Pdx1. This combination dramatically increased the level and timing of maximal <em>Ins1</em> mRNA expression to approximately 100% of that found in the βTC6 insulinoma cell line. Insulin protein and C-peptide expression was confirmed by immunohistochemistry staining. These inductive effects were restricted to c-kit<b><sup>+</sup></b> endoderm enriched EB-derived populations suggesting that Pdx1/Ngn3 functions after the specification of pancreatic endoderm. Although insulin secretion was stimulated by various insulin secretagogues, these cells had only limited glucose response. Microarray analysis was used to evaluate the expression of a broad spectrum of pancreatic endocrine cell-related genes as well as genes associated with glucose responses. Taken together, these findings demonstrate the utility of manipulating <em>Pdx1</em> and <em>Ngn3</em> expression in a stage-specific manner as an important new strategy for the efficient generation of functionally immature insulin-producing β-islet cells from ES cells.</p> </div>", "links"=>[], "tags"=>["pdx1", "ngn3", "overexpression", "enhances", "pancreatic", "differentiation", "es", "cell-derived", "endoderm"], "article_id"=>133367, "categories"=>["Physiology", "Chemistry", "Cell Biology", "Developmental Biology"], "users"=>["Atsushi Kubo", "Robert Stull", "Mitsuaki Takeuchi", "Kristina Bonham", "Valérie Gouon-Evans", "Masayuki Sho", "Masayuki Iwano", "Yoshihiko Saito", "Gordon Keller", "Ralph Snodgrass"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0024058.s001", "https://dx.doi.org/10.1371/journal.pone.0024058.s002", "https://dx.doi.org/10.1371/journal.pone.0024058.s003", "https://dx.doi.org/10.1371/journal.pone.0024058.s004"], "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Pdx1_and_Ngn3_Overexpression_Enhances_Pancreatic_Differentiation_of_Mouse_ES_Cell_Derived_Endoderm_Population/133367", "title"=>"Pdx1 and Ngn3 Overexpression Enhances Pancreatic Differentiation of Mouse ES Cell-Derived Endoderm Population", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-09-13 00:56:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/736209"], "description"=>"<p>Tet-pdx1/ngn3 ES cells were cultured according to Protocol #2, with BMP4. <i>Pdx1</i> and <i>Ngn3</i> were induced with Dox (Dox<sup>+</sup>) or without (Dox<sup>−</sup>) at day 4, and gene expression was analyzed from day 9–16 by RT-PCR and compared to βTC6 mRNA. (A) Secretory proteins and liver/intestine related-genes. (B) Insulin processing genes and glucose sensing genes. (C) Pancreas related-transcriptional factors.</p>", "links"=>[], "tags"=>["pancreas-related"], "article_id"=>406556, "categories"=>["Physiology", "Chemistry", "Cell Biology", "Developmental Biology"], "users"=>["Atsushi Kubo", "Robert Stull", "Mitsuaki Takeuchi", "Kristina Bonham", "Valérie Gouon-Evans", "Masayuki Sho", "Masayuki Iwano", "Yoshihiko Saito", "Gordon Keller", "Ralph Snodgrass"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024058.g003", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Time_course_of_pancreas_related_gene_expression_/406556", "title"=>"Time course of pancreas-related gene expression.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-13 01:49:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/736362"], "description"=>"<p>Tet-pdx1/ngn3 ES cells were cultured with Dox (Dox<sup>+</sup>) or without (Dox<sup>−</sup>) according to Protocol #3, including B27 supplement formulated with or without RA as indicated. (A) N2 supplement was added to the indicated groups from the beginning through day 14. B27(+RA), indicated by “+”, or B27(−RA), indicated by “−”, was included as a supplement from either day 0–4 or from day 4–14 as indicated. <i>Ins1</i> mRNA levels at day 14 were quantified by real time PCR and normalized to βTC6 levels. (B) Tet-pdx1/ngn3 ES cells were cultured with Dox (Dox<sup>+</sup>) or without (Dox<sup>−</sup>) according to Protocol #3 for 18 days. EBs were trypsinized to make single cell suspensions and cytoplasmic insulin was detected by immunostaining and analyzed by FACS. (C) EBs were cultured according to Protocol #3 for 18 days with or without Dox, after which the media was replaced with fresh medium for 24 hours and supernatants were harvested. C-peptide, glucagon and somatostatin were measured by either RIA (C-peptide) or EIA (glucagon, somatostatin) as described in Materials & <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0024058#s4\" target=\"_blank\">Methods</a>. (D) EBs cultured according to Protocol #3 for 19 days were resuspended in HKRB buffer and stimulated with KCl (30 mM), Forskolin (10 M) or IBMX (0.5 mM) for 1 hour. Supernatants were harvested and C-peptide was measured by RIA. For the Dox<sup>−</sup> samples in panels C & D, C-peptide and somatostatin values were not detectable above background. The data presented are mean of three independent experiments; the error bars represent the SEM. *p<0.05 as compared with Dox (−), **p<0.05 as compared with Dox(+).</p>", "links"=>[], "tags"=>["n2", "ra", "supplements", "increases"], "article_id"=>406702, "categories"=>["Physiology", "Chemistry", "Cell Biology", "Developmental Biology"], "users"=>["Atsushi Kubo", "Robert Stull", "Mitsuaki Takeuchi", "Kristina Bonham", "Valérie Gouon-Evans", "Masayuki Sho", "Masayuki Iwano", "Yoshihiko Saito", "Gordon Keller", "Ralph Snodgrass"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0024058.g004", "stats"=>{"downloads"=>4, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Deletion_of_N2_and_RA_supplements_increases_Ins1_expression_/406702", "title"=>"Deletion of N2 and RA supplements increases <i>Ins1</i> expression.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-13 01:51:42"}

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