Adipose Stromal Cells Contain Phenotypically Distinct Adipogenic Progenitors Derived from Neural Crest
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{"title"=>"Adipose stromal cells contain phenotypically distinct adipogenic progenitors derived from neural crest", "type"=>"journal", "authors"=>[{"first_name"=>"Yoshihiro", "last_name"=>"Sowa", "scopus_author_id"=>"6603762044"}, {"first_name"=>"Tetsuya", "last_name"=>"Imura", "scopus_author_id"=>"7103190623"}, {"first_name"=>"Toshiaki", "last_name"=>"Numajiri", "scopus_author_id"=>"12782294600"}, {"first_name"=>"Kosuke", "last_name"=>"Takeda", "scopus_author_id"=>"56079867200"}, {"first_name"=>"Yo", "last_name"=>"Mabuchi", "scopus_author_id"=>"23989018100"}, {"first_name"=>"Yumi", "last_name"=>"Matsuzaki", "scopus_author_id"=>"7201743234"}, {"first_name"=>"Kenichi", "last_name"=>"Nishino", "scopus_author_id"=>"35608537900"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"372407332", "scopus"=>"2-s2.0-84896726750", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pmid"=>"24391913", "sgr"=>"84896726750", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0084206"}, "id"=>"82273c91-cb89-3658-8bad-6127d081883d", "abstract"=>"Recent studies have shown that adipose-derived stromal/stem cells (ASCs) contain phenotypically and functionally heterogeneous subpopulations of cells, but their developmental origin and their relative differentiation potential remain elusive. In the present study, we aimed at investigating how and to what extent the neural crest contributes to ASCs using Cre-loxP-mediated fate mapping. ASCs harvested from subcutaneous fat depots of either adult P0-Cre/or Wnt1-Cre/Floxed-reporter mice contained a few neural crest-derived ASCs (NCDASCs). This subpopulation of cells was successfully expanded in vitro under standard culture conditions and their growth rate was comparable to non-neural crest derivatives. Although NCDASCs were positive for several mesenchymal stem cell markers as non-neural crest derivatives, they exhibited a unique bipolar or multipolar morphology with higher expression of markers for both neural crest progenitors (p75NTR, Nestin, and Sox2) and preadipocytes (CD24, CD34, S100, Pref-1, GATA2, and C/EBP-delta). NCDASCs were able to differentiate into adipocytes with high efficiency but their osteogenic and chondrogenic potential was markedly attenuated, indicating their commitment to adipogenesis. In vivo, a very small proportion of adipocytes were originated from the neural crest. In addition, p75NTR-positive neural crest-derived cells were identified along the vessels within the subcutaneous adipose tissue, but they were negative for mural and endothelial markers. These results demonstrate that ASCs contain neural crest-derived adipocyte-restricted progenitors whose phenotype is distinct from that of non-neural crest derivatives.", "link"=>"http://www.mendeley.com/research/adipose-stromal-cells-contain-phenotypically-distinct-adipogenic-progenitors-derived-neural-crest", "reader_count"=>35, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Student > Doctoral Student"=>3, "Researcher"=>9, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>3, "Student > Master"=>4, "Other"=>2, "Student > Bachelor"=>1, "Lecturer"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Student > Doctoral Student"=>3, "Researcher"=>9, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>3, "Student > Master"=>4, "Other"=>2, "Student > Bachelor"=>1, "Lecturer"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>23, "Medicine and Dentistry"=>5, "Neuroscience"=>1, "Veterinary Science and Veterinary Medicine"=>1, "Chemistry"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>5}, "Neuroscience"=>{"Neuroscience"=>1}, "Chemistry"=>{"Chemistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>23}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Unspecified"=>{"Unspecified"=>2}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"United States"=>1, "Brazil"=>1, "France"=>1, "Germany"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1334673"], "description"=>"<p><b><i>A</i></b>. Schematic diagram of the Cre-loxP-mediated fate mapping of NC-derived cells. Either P0-Cre or Wnt1-Cre transgenic mice are crossed with CAG-CAT-EGFP mice to generate NC-specific Cre/Foxed-Reporter (FR) mice in which NC-derived cells can be traced by the expression of the reporter protein GFP. <b><i>B</i></b>. Flow cytometry profiles of ASCs from adult Cre/FR mice. The x axis is GFP fluorescent intensity, and the y axis is the side scatter channel (SSC). ASCs from non-transgenic controls served as a gating control. The proportions of GFP+ cells per total cells were 0.98±0.24% and 1.48±0.35% in P0-Cre/FR and in Wnt1-Cre/FR mice, respectively. <b><i>C</i></b>. Phase contrast and fluorescent micrographs of second passage ASC cultures isolated from adult P0-Cre/FR (<i>left</i>) and Wnt1-Cre/FR mice (<i>right</i>). The majority of GFP+ cells possess small soma with long slender processes (<i>arrow in bottom</i>), whereas a few cells show a flat/polygonal shape similar to GFP- ASCs (<i>arrowhead</i>). Scale bar  = 50 µm. <b><i>D</i></b>. The proportions of GFP+ cells in ASC cultures from P0-Cre/FR mice of different ages (1 week-, 3 week-, and 16 week-old) at different passages (from passage 0 to 6). Data are shown as the mean + SEM of 6 independent cultures. <b><i>E</i></b>. Growth curves of GFP+ and GFP− cells sorted from second passage ASCs of P0-Cre/FR mice. Results are shown as relative changes to the cell number on day 0 (after sorting). There was no significant difference in the population doubling time between GFP+ and GFP− cells. Data are shown as the mean ± SEM of 3 independent experiments for each condition.</p>", "links"=>[], "tags"=>["developmental biology", "stem cells", "mesenchymal stem cells", "Cell differentiation", "Cell fate determination", "Model organisms", "Animal models", "mouse", "Molecular cell biology", "Cellular types", "Adult stem cells", "neural", "crest-derived", "cells"], "article_id"=>891045, "categories"=>["Biological Sciences"], "users"=>["Yoshihiro Sowa", "Tetsuya Imura", "Toshiaki Numajiri", "Kosuke Takeda", "Yo Mabuchi", "Yumi Matsuzaki", "Kenichi Nishino"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0084206.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Contribution_of_neural_crest_derived_cells_to_adult_ASCs_/891045", "title"=>"Contribution of neural crest-derived cells to adult ASCs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-31 04:47:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/1334676"], "description"=>"<p><b><i>A</i></b>. Quantification of surface marker expression in both GFP+ and GFP− ASCs of either P0-Cre/FR or Wnt1-Cre/FR mice with flow cytometric analysis. The majority of both GFP+ and GFP− cells expressed MSC markers including CD29, CD44, CD90, CD105, and Sca-1. <b><i>B</i></b>. The proportion of both CD24- and CD34-positive cells in the GFP+ population was also higher, and the proportion of double-positive cells in the GFP+ population was more than five-fold higher compared to those in GFP− cells. Representative flow cytometry profiles of CD24/CD34 double-positive cells from P0-Cre/FR mice are shown. <b><i>C</i></b>. The GFP+ population had a significantly higher proportion of p75NTR-positive cells. Data (<i>A–C</i>) are shown as the mean + SEM of 4 independent experiments for each condition. *<i>p</i><0.05 versus GFP− cells, <i>t</i> test. <b><i>D</i></b>. Immunofluorescent staining for p75NTR, S100, Nestin, GFAP, and fibronectin (<i>red</i>) of either P0-Cre/FR ASCs (<i>upper five panels</i>) or Wnt1-Cre/FR (<i>lower two panels</i>) shows that the majority of GFP+ cells (<i>green</i>) co-expressed p75NTR, S100, and Nestin (<i>arrow</i>) but were negative for GFAP and fibronectin. A few GFP-negative but p75NTR- S100-, or Nestin-positive cells were also observed (<i>arrowhead</i>). Note that the majority of GFP− cells were positive for fibronectin. Scale bar  = 50 µm. <i>E</i>. RT-qPCR analysis for pluripotent markers <i>Sox2, Nanog</i>, and <i>Oct3/4</i> on FACS-purified GFP− and GFP+ cells from P0-Cre/FR mice. Results are normalized based on <i>GAPDH</i> expression and shown as relative changes to GFP− cells. Data are shown as the mean + SEM of 3–4 independent experiments for each condition.</p>", "links"=>[], "tags"=>["developmental biology", "stem cells", "mesenchymal stem cells", "Cell differentiation", "Cell fate determination", "Model organisms", "Animal models", "mouse", "Molecular cell biology", "Cellular types", "Adult stem cells", "neural", "crest-derived"], "article_id"=>891048, "categories"=>["Biological Sciences"], "users"=>["Yoshihiro Sowa", "Tetsuya Imura", "Toshiaki Numajiri", "Kosuke Takeda", "Yo Mabuchi", "Yumi Matsuzaki", "Kenichi Nishino"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0084206.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Characterization_of_neural_crest_derived_ASCs_/891048", "title"=>"Characterization of neural crest-derived ASCs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-31 04:47:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/1334681"], "description"=>"<p><b><i>A</i></b>. Phase contrast and fluorescent images show that both GFP+ (<i>arrow</i>) and GFP− ASCs (<i>arrowhead</i>) from P0-Cre/FR mice contain lipid droplets after adipogenic differentiation. Scale bar  = 50 µm. <b><i>B</i></b>. FACS-purified GFP+ cells are positive for both perilipin immunostaining (<i>top left, top right, and bottom left</i>) and Oil red O staining (<i>bottom right</i>) after adipogenic differentiation. Nuclei were stained with DAPI (<i>blue</i>). Scale bar  = 50 µm. <b><i>C</i></b>. Representative images and quantification of adipogenic differentiation of FACS-purified GFP+ and GFP− cells. The percentage of perilipin-positive cells per total cells was more than 1.5-fold higher in the GFP+ cells than that of the GFP-cells. Data are shown as the mean + SEM of 4 independent experiments for each condition. *<i>p</i><0.05 versus GFP− cells, <i>t</i> test. <b><i>D</i></b>. RT-qPCR analysis for preadipocyte markers <i>Pref-1, C/EBPδ</i>, and <i>GATA2</i>, as well as for mature adipocyte markers <i>PPARγ</i> and <i>aP2</i> on purified GFP− and GFP+ cells before or after (<i>adipo</i>) adipogenic induction. Results are normalized based on <i>GAPDH</i> expression and shown as relative changes to undifferentiated GFP− cells. Data are shown as the mean + SEM of 3–4 independent experiments for each condition.</p>", "links"=>[], "tags"=>["developmental biology", "stem cells", "mesenchymal stem cells", "Cell differentiation", "Cell fate determination", "Model organisms", "Animal models", "mouse", "Molecular cell biology", "Cellular types", "Adult stem cells", "neural", "crest-derived"], "article_id"=>891053, "categories"=>["Biological Sciences"], "users"=>["Yoshihiro Sowa", "Tetsuya Imura", "Toshiaki Numajiri", "Kosuke Takeda", "Yo Mabuchi", "Yumi Matsuzaki", "Kenichi Nishino"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0084206.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Adipogenic_potential_of_neural_crest_derived_ASCs_/891053", "title"=>"Adipogenic potential of neural crest-derived ASCs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-31 04:47:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/1334686"], "description"=>"<p><b><i>A</i></b>. Bright-field images of alizarin staining (<i>top</i>) and fluorescent images of osteopontin immunostaning (<i>red in bottom</i>) in FACS-purified GFP- and GFP+ cells after osteogenic induction. Nuclei were stained with DAPI (<i>blue</i>). Scale bar  = 50 µm. <b><i>B</i></b>. The osteopontin-positive area was measured and expressed as a percentage of the total area. Data are shown as mean +SEM, n = 3. **<i>p</i><0.01 versus GFP− cells, <i>t</i> test. <b><i>C</i></b>. Bright-field images of Alcian blue staining in FACS-purified GFP+ and GFP− cells after chondrogenic induction. Scale bar = 100 µm. <b><i>D</i></b>. RT-qPCR analysis for chondrogenic markers <i>Aggrecan, COL2a1</i>, and <i>Sox9</i> in the GFP− and the GFP+ cells after chondrogenic differentiation. Results are normalized based on <i>GAPDH</i> expression and shown as relative changes to GFP-cells. Data are shown as the mean + SEM of 3–4 independent experiments for each condition.</p>", "links"=>[], "tags"=>["developmental biology", "stem cells", "mesenchymal stem cells", "Cell differentiation", "Cell fate determination", "Model organisms", "Animal models", "mouse", "Molecular cell biology", "Cellular types", "Adult stem cells", "chondrogenic", "neural", "crest-derived"], "article_id"=>891058, "categories"=>["Biological Sciences"], "users"=>["Yoshihiro Sowa", "Tetsuya Imura", "Toshiaki Numajiri", "Kosuke Takeda", "Yo Mabuchi", "Yumi Matsuzaki", "Kenichi Nishino"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0084206.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Osteogenic_and_chondrogenic_potential_of_neural_crest_derived_ASCs_/891058", "title"=>"Osteogenic and chondrogenic potential of neural crest-derived ASCs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-31 04:47:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/1334688"], "description"=>"<p>Confocal micrographs of the reporter protein GFP (<i>green</i>) combined with immunofluorescence of various markers (<i>red</i>) in the adult subcutaneous tissue of either P0-Cre/FR (<i>A, B, D–I</i>) or Wnt1-Cre/FR (<i>C, J</i>) mice. <b><i>A–A″</i></b>. A small portion of perilipin-positive adipocytes expressed GFP in the cephalic region. <b><i>B</i></b>. Peripheral nerve tissue was GFP+. <b><i>C</i></b>. GFP+ cells with slender processes were identified in the stroma of both cephalic and trunk regions. <b><i>D–J</i></b>. These cells (<i>arrow</i>) were localized along the vessels or occasionally in the vicinity to GFP+ adipocytes (<i>arrowhead in E</i>). They were negative for an endothelial marker CD31 (<i>D</i>), mural markers PDGFRβ and αSMA (<i>E, F</i>), and a glial marker GFAP (<i>G</i>), but positive for p75NTR and S100 (<i>H–J</i>). Nuclei were stained with DAPI (<i>blue, D–F, H–J</i>). Scale bar = 20 µm (<i>A, B</i>), 10 µm (<i>C–J</i>).</p>", "links"=>[], "tags"=>["developmental biology", "stem cells", "mesenchymal stem cells", "Cell differentiation", "Cell fate determination", "Model organisms", "Animal models", "mouse", "Molecular cell biology", "Cellular types", "Adult stem cells", "localization", "neural", "crest-derived", "cells", "subcutaneous", "adipose"], "article_id"=>891060, "categories"=>["Biological Sciences"], "users"=>["Yoshihiro Sowa", "Tetsuya Imura", "Toshiaki Numajiri", "Kosuke Takeda", "Yo Mabuchi", "Yumi Matsuzaki", "Kenichi Nishino"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0084206.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_In_vivo_localization_of_neural_crest_derived_cells_in_the_subcutaneous_adipose_tissue_/891060", "title"=>"<i>In vivo</i> localization of neural crest-derived cells in the subcutaneous adipose tissue.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-31 04:47:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/1334689"], "description"=>"<p>Various kinds of stem/progenitor cells are present in the putative perivascular niche of adipose tissue, such as tissue-resident mesoderm-derived cells, circulating bone marrow-derived cells <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0084206#pone.0084206-Majka1\" target=\"_blank\">[12]</a>, and NC-derived cells (“Fat tissue <i>in vivo</i>”). Endothelial cells could be an alternative source <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0084206#pone.0084206-Slukvin1\" target=\"_blank\">[11]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0084206#pone.0084206-Medici1\" target=\"_blank\">[42]</a>. Although the roles of these different cell populations <i>in vivo</i> remain largely unknown, they participate in generating phenotypic and functional diversity of ASCs in culture. NC-derived cells exhibit unique morphological and antigenic features and are largely restricted to the adipogenic lineage. The relationship among multipotent stem cells, osteogenic progenitors, and chondrogenic progenitors and their developmental origins are currently unknown (“<i>Ex vivo</i>”). Detailed characterization of different cell subpopulations is important for effective therapeutic application of ASCs.</p>", "links"=>[], "tags"=>["developmental biology", "stem cells", "mesenchymal stem cells", "Cell differentiation", "Cell fate determination", "Model organisms", "Animal models", "mouse", "Molecular cell biology", "Cellular types", "Adult stem cells", "heterogeneous", "populations", "origins", "adipose"], "article_id"=>891061, "categories"=>["Biological Sciences"], "users"=>["Yoshihiro Sowa", "Tetsuya Imura", "Toshiaki Numajiri", "Kosuke Takeda", "Yo Mabuchi", "Yumi Matsuzaki", "Kenichi Nishino"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0084206.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_proposed_model_showing_heterogeneous_stem_progenitor_cell_populations_of_different_origins_in_adipose_tissue_/891061", "title"=>"A proposed model showing heterogeneous stem/progenitor cell populations of different origins in adipose tissue.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-31 04:47:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/1334690"], "description"=>"<p>RT-PCR primer sequences.</p>", "links"=>[], "tags"=>["developmental biology", "stem cells", "mesenchymal stem cells", "Cell differentiation", "Cell fate determination", "Model organisms", "Animal models", "mouse", "Molecular cell biology", "Cellular types", "Adult stem cells", "primer"], "article_id"=>891062, "categories"=>["Biological Sciences"], "users"=>["Yoshihiro Sowa", "Tetsuya Imura", "Toshiaki Numajiri", "Kosuke Takeda", "Yo Mabuchi", "Yumi Matsuzaki", "Kenichi Nishino"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0084206.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RT_PCR_primer_sequences_/891062", "title"=>"RT-PCR primer sequences.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-12-31 04:47:52"}

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Relative Metric

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